PIEZO2 gene and its role in the development of distal arthrogryposis: A literature review

Abstract

BACKGROUND: PIEZO1 and PIEZO2 are mechanosensitive ion channel proteins; in humans, they are encoded by genes with identical names. PIEZO proteins convert mechanical signals into biochemical cellular responses following transduction. Recent data highlight the importance of this family of ion channel proteins in the regulation of physiological processes; however, many mechanisms remain unknown. Modern studies have proven that PIEZO2 mutations lead to the development of various forms of distal arthrogryposis.

AIM: To analyze publications containing information on PIEZO2 gene and its role in the development of distal forms of arthrogryposis.

MATERIALS AND METHODS: This study analyzed the results of a literature search in the open scientific literature databases of PubMed, Cochrane Library, and eLibrary. Consequently, 40 foreign, and domestic scientific sources were extracted from 1969 to 2022.

RESULTS: This study showed the relationship between PIEZO2 mutations and the development of the distal forms of arthrogryposis. The study also presented the types of distal arthrogryposis and their clinical manifestations depending on the mutation of this gene. PIEZO2 mutations with decreased function cause distal arthrogryposis with impaired proprioception and taction (autosomal recessive type of inheritance). PIEZO2 mutations with gain-of-function cause distal arthrogryposis of types 3 and 5 (autosomal dominant inheritance).

CONCLUSIONS: An integrated approach to the diagnosis and molecular genetic study will allow us to choose the best techniques and treatment of patients with this pathology. The results are useful for doctors of various specialties.

Keywords

distal arthrogryposis / PIEZO2 gene / mutations

References

[1] Szczot M, Nickolls AR, Lam RM, et al. The form and function of PIEZO2. Annu Rev Biochem. 2021;90:507–534. DOI: 10.1146/annurev-biochem-081720-023244

[2] Szczot M., Nickolls A.R., Lam R.M., et al. The form and function of PIEZO2 // Ann. Rev. Biochem. 2021. Vol. 20. No. 90. P. 507–534. DOI: 10.1146/annurev-biochem-081720-023244

[3] Szczot M, Nickolls AR, Lam RM, et al. The form and function of PIEZO2. Annu Rev Biochem. 2021;90:507–534. DOI: 10.1146/annurev-biochem-081720-023244

[4] Assaraf E, Blecher R, Heinemann-Yerushalmi L, et al. PIEZO2 expressed in proprioceptive neurons is essential for skeletal integrity. Nat Commun. 2020;11(1). DOI: 10.1038/s41467-020-16971-6

[5] Assaraf E., Blecher R., Heinemann-Yerushalmi L., et al. PIEZO2 expressed in proprioceptive neurons is essential for skeletal integrity // Nat. Commun. 2020. Vol. 11. No. 1. DOI: 10.1038/s41467-020-16971-6

[6] Assaraf E, Blecher R, Heinemann-Yerushalmi L, et al. PIEZO2 expressed in proprioceptive neurons is essential for skeletal integrity. Nat Commun. 2020;11(1). DOI: 10.1038/s41467-020-16971-6

[7] Coste B, Mathur J, Schmidt M, et al. PIEZO1 and PIEZO2 are essential components of distinct mechanically activated cation channels. Science. 2010;330(6000):55–60. DOI: 10.1126/science.1193270

[8] Coste B., Mathur J., Schmidt M., et al. PIEZO1 and PIEZO2 are essential components of distinct mechanically activated cation channels // Science. 2010. Vol. 330. No. 6000. P. 55–60. DOI: 10.1126/science.1193270

[9] Coste B, Mathur J, Schmidt M, et al. PIEZO1 and PIEZO2 are essential components of distinct mechanically activated cation channels. Science. 2010;330(6000):55–60. DOI: 10.1126/science.1193270

[10] Coste B, Xiao B, Santos JS, et al. PIEZO proteins are pore-forming subunits of mechanically activated channels. Nature. 2012;483(7388):176–181. DOI: 10.1038/nature10812

[11] Coste B., Xiao B., Santos J.S., et al. PIEZO proteins are pore-forming subunits of mechanically activated channels // Nature. 2012. Vol. 483. No. 7388. P. 176–181. DOI: 10.1038/nature10812

[12] Coste B, Xiao B, Santos JS, et al. PIEZO proteins are pore-forming subunits of mechanically activated channels. Nature. 2012;483(7388):176–181. DOI: 10.1038/nature10812

[13] Bamshad M, van Heest AE, Pleasure D. Arthrogryposis: a review and update. J Bone Joint Surg Am. 2009;91(Suppl 4):40–46. DOI: 10.2106/JBJS.I.00281

[14] Bamshad M., van Heest A.E., Pleasure D. Arthrogryposis: a review and update // J. Bone Joint Surg. Am. 2009. Vol. 91. Suppl. 4. P. 40–46. DOI: 10.2106/JBJS.I.00281

[15] Bamshad M, van Heest AE, Pleasure D. Arthrogryposis: a review and update. J Bone Joint Surg Am. 2009;91(Suppl 4):40–46. DOI: 10.2106/JBJS.I.00281

[16] Gordon H, Davies D, Berman M. Camptodactyly, cleft palate, and club foot. A syndrome showing the autosomal-dominant pattern of inheritance. J Med Genet. 1969;6(3):266–274. DOI: 10.1136/jmg.6.3.266

[17] Gordon H., Davies D., Berman M. Camptodactyly, cleft palate, and club foot. A syndrome showing the autosomal-dominant pattern of inheritance // J. Med. Genet. 1969. Vol. 6. No. 3. P. 266–274. DOI: 10.1136/jmg.6.3.266

[18] Gordon H, Davies D, Berman M. Camptodactyly, cleft palate, and club foot. A syndrome showing the autosomal-dominant pattern of inheritance. J Med Genet. 1969;6(3):266–274. DOI: 10.1136/jmg.6.3.266

[19] Say B, Barber DH, Thompson RC, et al. The Gordon syndrome. J Med Genet. 1980;17(5). DOI: 10.1136/jmg.17.5.405

[20] Say B., Barber D.H., Thompson R.C., et al. The Gordon syndrome // J. Med. Genet. 1980. Vol. 17. No. 5. DOI: 10.1136/jmg.17.5.405

[21] Say B, Barber DH, Thompson RC, et al. The Gordon syndrome. J Med Genet. 1980;17(5). DOI: 10.1136/jmg.17.5.405

[22] Hall JG, Reed SD, Greene G. The distal arthrogryposes: delineation of new entities – review and nosologic discussion. Am J Med Genet. 1982;11(2):185–239. DOI: 10.1002/ajmg.1320110208

[23] Hall J.G., Reed S.D., Greene G. The distal arthrogryposes: delineation of new entities – review and nosologic discussion // Am. J. Med. Genet. 1982. Vol. 11. No. 2. P. 185–239. DOI: 10.1002/ajmg.1320110208

[24] Hall JG, Reed SD, Greene G. The distal arthrogryposes: delineation of new entities – review and nosologic discussion. Am J Med Genet. 1982;11(2):185–239. DOI: 10.1002/ajmg.1320110208

[25] Ioan DM, Belengeanu V, Maximilian C, et al. Distal arthrogryposis with autosomal dominant inheritance and reduced penetrance in females: the Gordon syndrome. Clin Genet. 1993;43(6):300–302. DOI: 10.1111/j.1399-0004.1993.tb03822.x

[26] Ioan D.M., Belengeanu V., Maximilian C., et al. Distal arthrogryposis with autosomal dominant inheritance and reduced penetrance in females: the Gordon syndrome // Clin. Genet. 1993. Vol. 43. No. 6. P. 300–302. DOI: 10.1111/j.1399-0004.1993.tb03822.x

[27] Ioan DM, Belengeanu V, Maximilian C, et al. Distal arthrogryposis with autosomal dominant inheritance and reduced penetrance in females: the Gordon syndrome. Clin Genet. 1993;43(6):300–302. DOI: 10.1111/j.1399-0004.1993.tb03822.x

[28] Wild A, Schillians N, Kumar M, et al. Scoliosis in Gordon’s syndrome. Eur Spine J. 2001;10(5):458–460. DOI: 10.1007/s005860100265

[29] Wild A., Schillians N., Kumar M., et al. Scoliosis in Gordon’s syndrome // Eur. Spine J. 2001. Vol. 10. No. 5. P. 458–460. DOI: 10.1007/s005860100265

[30] Wild A, Schillians N, Kumar M, et al. Scoliosis in Gordon’s syndrome. Eur Spine J. 2001;10(5):458–460. DOI: 10.1007/s005860100265

[31] Botha SJ, Bütow KW. Gordon syndrome: literature review and a report of two cases. Cleft Palate Craniofac J. 2015;52(1):e18–22. DOI: 10.1597/13-075

[32] Botha S.J., Bütow K.W. Gordon syndrome: literature review and a report of two cases // Cleft Palate Craniofac. J. 2015. Vol. 52. No. 1. P. e18–22. DOI: 10.1597/13-075

[33] Botha SJ, Bütow KW. Gordon syndrome: literature review and a report of two cases. Cleft Palate Craniofac J. 2015;52(1):e18–22. DOI: 10.1597/13-075

[34] Alisch F, Weichert A, Kalache K, et al. Familial Gordon syndrome associated with a PIEZO2 mutation. Am J Med Genet A. 2017;173(1):254–259. DOI: 10.1002/ajmg.a.37997

[35] Alisch F., Weichert A., Kalache K., et al. Familial Gordon syndrome associated with a PIEZO2 mutation // Am. J. Med. Genet. A. 2017. Vol. 173. No. 1. P. 254–259. DOI: 10.1002/ajmg.a.37997

[36] Alisch F, Weichert A, Kalache K, et al. Familial Gordon syndrome associated with a PIEZO2 mutation. Am J Med Genet A. 2017;173(1):254–259. DOI: 10.1002/ajmg.a.37997

[37] Roomaney IA, Walters J, Spencer C, et al. Gordon syndrome: dental implications and a case report. Spec Care Dentist. 2021;41(6):727–734. DOI: 10.1111/scd.12615

[38] Roomaney I.A., Walters J., Spencer C., et al. Gordon syndrome: dental implications and a case report // Spec. Care Dentist. 2021. Vol. 41. No. 6. P. 727–734. DOI: 10.1111/scd.12615

[39] Roomaney IA, Walters J, Spencer C, et al. Gordon syndrome: dental implications and a case report. Spec Care Dentist. 2021;41(6):727–734. DOI: 10.1111/scd.12615

[40] Halal F, Fraser FC. Camptodactyly, cleft palate, and club foot (the Gordon syndrome). A report of a large pedigree. J Med Genet. 1979;16(2):149–150. DOI: 10.1136/jmg.16.2.149

[41] Halal F., Fraser F.C. Camptodactyly, cleft palate, and club foot (the Gordon syndrome). A report of a large pedigree // J. Med. Genet. 1979. Vol. 16. No. 2. P. 149–150. DOI: 10.1136/jmg.16.2.149

[42] Halal F, Fraser FC. Camptodactyly, cleft palate, and club foot (the Gordon syndrome). A report of a large pedigree. J Med Genet. 1979;16(2):149–150. DOI: 10.1136/jmg.16.2.149

[43] McMillin MJ, Beck AE, Chong JX, et al. Mutations in PIEZO2 cause Gordon syndrome, Marden-Walker syndrome, and distal arthrogryposis type 5. Am J Hum Genet. 2014;94(5):734–744. DOI: 10.1016/j.ajhg.2014.03.015

[44] McMillin M.J., Beck A.E., Chong J.X., et al. Mutations in PIEZO2 cause Gordon syndrome, Marden-Walker syndrome, and distal arthrogryposis type 5 // Am. J. Hum. Genet. 2014. Vol. 94. No. 5. P. 734–744. DOI: 10.1016/j.ajhg.2014.03.015

[45] McMillin MJ, Beck AE, Chong JX, et al. Mutations in PIEZO2 cause Gordon syndrome, Marden-Walker syndrome, and distal arthrogryposis type 5. Am J Hum Genet. 2014;94(5):734–744. DOI: 10.1016/j.ajhg.2014.03.015

[46] Becker K, Splitt M. A family with distal arthrogryposis and cleft palate: possible overlap between Gordon syndrome and Aase-Smith syndrome. Clin Dysmorphol. 2001;10(1):41–45. DOI: 10.1097/00019605-200101000-00009

[47] Becker K., Splitt M. A family with distal arthrogryposis and cleft palate: possible overlap between Gordon syndrome and Aase-Smith syndrome // Clin. Dysmorphol. 2001. Vol. 10. No. 1. P. 41–45. DOI: 10.1097/00019605-200101000-00009

[48] Becker K, Splitt M. A family with distal arthrogryposis and cleft palate: possible overlap between Gordon syndrome and Aase-Smith syndrome. Clin Dysmorphol. 2001;10(1):41–45. DOI: 10.1097/00019605-200101000-00009

[49] Lai MM, Tettenborn MA, Hall JG, et al. A new form of autosomal dominant arthrogryposis. J Med Genet. 1991;28(10):701–703. DOI: 10.1136/jmg.28.10.701

[50] Lai M.M., Tettenborn M.A., Hall J.G., et al. A new form of autosomal dominant arthrogryposis // J. Med. Genet. 1991. Vol. 28. No. 10. P. 701–703. DOI: 10.1136/jmg.28.10.701

[51] Lai MM, Tettenborn MA, Hall JG, et al. A new form of autosomal dominant arthrogryposis. J Med Genet. 1991;28(10):701–703. DOI: 10.1136/jmg.28.10.701

[52] Schrander-Stumpel CT, Höweler CJ, Reekers AD, et al. Arthrogryposis, ophthalmoplegia, and retinopathy: confirmation of a new type of arthrogryposis. J Med Genet. 1993;30(1):78–80. DOI: 10.1136/jmg.30.1.78

[53] Schrander-Stumpel C.T., Höweler C.J., Reekers A.D., et al. Arthrogryposis, ophthalmoplegia, and retinopathy: confirmation of a new type of arthrogryposis // J. Med. Genet. 1993. Vol. 30. No. 1. P. 78–80. DOI: 10.1136/jmg.30.1.78

[54] Schrander-Stumpel CT, Höweler CJ, Reekers AD, et al. Arthrogryposis, ophthalmoplegia, and retinopathy: confirmation of a new type of arthrogryposis. J Med Genet. 1993;30(1):78–80. DOI: 10.1136/jmg.30.1.78

[55] Friedman BD, Heidenreich RA. Distal arthrogryposis type IIB: further clinical delineation and 54-year follow-up of an index case. Am J Med Genet. 1995;58(2):125–127. DOI: 10.1002/ajmg.1320580207

[56] Friedman B.D., Heidenreich R.A. Distal arthrogryposis type IIB: further clinical delineation and 54-year follow-up of an index case // Am. J. Med. Genet. 1995. Vol. 58. No. 2. P. 125–127. DOI: 10.1002/ajmg.1320580207

[57] Friedman BD, Heidenreich RA. Distal arthrogryposis type IIB: further clinical delineation and 54-year follow-up of an index case. Am J Med Genet. 1995;58(2):125–127. DOI: 10.1002/ajmg.1320580207

[58] Pallotta R, Ehresmann T, Fusilli P. Occurrence of Dandy-Walker anomaly in a familial case of distal arthogryposis type IIB. Am J Med Genet. 2000;95(5):477–481. DOI: 10.1002/1096-8628(20001218)95:5<477::aid-ajmg13>3.0.co;2-m

[59] Pallotta R., Ehresmann T., Fusilli P. Occurrence of Dandy-Walker anomaly in a familial case of distal arthogryposis type IIB // Am. J. Med. Genet. 2000. Vol. 95. No. 5. P. 477–81. DOI: 10.1002/1096-8628(20001218)95:5<477::aid-ajmg13>3.0.co;2-m

[60] Pallotta R, Ehresmann T, Fusilli P. Occurrence of Dandy-Walker anomaly in a familial case of distal arthogryposis type IIB. Am J Med Genet. 2000;95(5):477–481. DOI: 10.1002/1096-8628(20001218)95:5<477::aid-ajmg13>3.0.co;2-m

[61] Beals RK, Weleber RG. Distal arthrogryposis 5: a dominant syndrome of peripheral contractures and ophthalmoplegia. Am J Med Genet A. 2004;131(1):67–70. DOI: 10.1002/ajmg.a.30289

[62] Beals R.K., Weleber R.G. Distal arthrogryposis 5: a dominant syndrome of peripheral contractures and ophthalmoplegia // Am. J. Med. Genet. A. 2004. Vol. 131. No. 1. P. 67–70. DOI: 10.1002/ajmg.a.30289

[63] Beals RK, Weleber RG. Distal arthrogryposis 5: a dominant syndrome of peripheral contractures and ophthalmoplegia. Am J Med Genet A. 2004;131(1):67–70. DOI: 10.1002/ajmg.a.30289

[64] Sahni J, Kaye SB, Fryer A, et al. Distal arthrogryposis type IIB: unreported ophthalmic findings. Am J Med Genet A. 2004;127A(1):35–39. DOI: 10.1002/ajmg.a.20634

[65] Sahni J., Kaye S.B., Fryer A., et al. Distal arthrogryposis type IIB: unreported ophthalmic findings // Am. J. Med. Genet. A. 2004. Vol. 127A. No. 1. P. 35–39. DOI: 10.1002/ajmg.a.20634

[66] Sahni J, Kaye SB, Fryer A, et al. Distal arthrogryposis type IIB: unreported ophthalmic findings. Am J Med Genet A. 2004;127A(1):35–39. DOI: 10.1002/ajmg.a.20634

[67] Williams MS, Elliott CG, Bamshad MJ. Pulmonary disease is a component of distal arthrogryposis type 5. Am J Med Genet A. 2007;143A(7):752–756. DOI: 10.1002/ajmg.a.31648

[68] Williams M.S., Elliott C.G., Bamshad M.J. Pulmonary disease is a component of distal arthrogryposis type 5 // Am. J. Med. Genet. A. 2007. Vol. 143A. No. 7. P. 752–756. DOI: 10.1002/ajmg.a.31648

[69] Williams MS, Elliott CG, Bamshad MJ. Pulmonary disease is a component of distal arthrogryposis type 5. Am J Med Genet A. 2007;143A(7):752–756. DOI: 10.1002/ajmg.a.31648

[70] Castori M, Rinaldi R, Barboni L, et al. Juvenile macular dystrophy and forearm pronation-supination restriction presenting with features of distal arthrogryposis type 5. Am J Med Genet A. 2009;149A(3):482–486. DOI: 10.1002/ajmg.a.32668

[71] Castori M., Rinaldi R., Barboni L., et al. Juvenile macular dystrophy and forearm pronation-supination restriction presenting with features of distal arthrogryposis type 5 // Am. J. Med. Genet. A. 2009. Vol. 149A. No. 3. P. 482–486. DOI: 10.1002/ajmg.a.32668

[72] Castori M, Rinaldi R, Barboni L, et al. Juvenile macular dystrophy and forearm pronation-supination restriction presenting with features of distal arthrogryposis type 5. Am J Med Genet A. 2009;149A(3):482–486. DOI: 10.1002/ajmg.a.32668

[73] Coste B, Houge G, Murray MF, et al. Gain-of-function mutations in the mechanically activated ion channel PIEZO2 cause a subtype of distal arthrogryposis. Proc Natl Acad Sci USA. 2013;110(12):4667–4672. DOI: 10.1073/pnas.1221400110

[74] Coste B., Houge G., Murray M.F., et al. Gain-of-function mutations in the mechanically activated ion channel PIEZO2 cause a subtype of distal arthrogryposis // Proc. Natl. Acad. Sci. USA. 2013. Vol. 110. No. 12. P. 4667–4472. DOI: 10.1073/pnas.1221400110

[75] Coste B, Houge G, Murray MF, et al. Gain-of-function mutations in the mechanically activated ion channel PIEZO2 cause a subtype of distal arthrogryposis. Proc Natl Acad Sci USA. 2013;110(12):4667–4672. DOI: 10.1073/pnas.1221400110

[76] Okubo M, Fujita A, Saito Y, et al. A family of distal arthrogryposis type 5 due to a novel PIEZO2 mutation. Am J Med Genet A. 2015;167A(5):1100–1106. DOI: 10.1002/ajmg.a.36881

[77] Okubo M., Fujita A., Saito Y., et al. A family of distal arthrogryposis type 5 due to a novel PIEZO2 mutation // Am. J. Med. Genet. A. 2015. Vol. 167A. No. 5. P. 1100–1106. DOI: 10.1002/ajmg.a.36881

[78] Okubo M, Fujita A, Saito Y, et al. A family of distal arthrogryposis type 5 due to a novel PIEZO2 mutation. Am J Med Genet A. 2015;167A(5):1100–1106. DOI: 10.1002/ajmg.a.36881

[79] Zapata-Aldana E, Al-Mobarak SB, Karp N, et al. Distal arthrogryposis type 5 and PIEZO2 novel variant in a Canadian family. Am J Med Genet A. 2019;179(6):1034–1041. DOI: 10.1002/ajmg.a.61143

[80] Zapata-Aldana E., Al-Mobarak S.B., Karp N., et al. Distal arthrogryposis type 5 and PIEZO2 novel variant in a Canadian family // Am. J. Med. Genet. A. 2019. Vol. 179. No. 6. P. 1034–1041. DOI: 10.1002/ajmg.a.61143

[81] Zapata-Aldana E, Al-Mobarak SB, Karp N, et al. Distal arthrogryposis type 5 and PIEZO2 novel variant in a Canadian family. Am J Med Genet A. 2019;179(6):1034–1041. DOI: 10.1002/ajmg.a.61143

[82] Serra G, Antona V, Cannata C, et al. Distal Arthrogryposis type 5 in an Italian family due to an autosomal dominant gain-of-function mutation of the PIEZO2 gene. Ital J Pediatr. 2022;48(1). DOI: 10.1186/s13052-022-01329-z

[83] Serra G., Antona V., Cannata C., et al. Distal arthrogryposis type 5 in an Italian family due to an autosomal dominant gain-of-function mutation of the PIEZO2 gene // Ital. J. Pediatr. 2022. Vol. 48. No. 1. P. 133. DOI: 10.1186/s13052-022-01329-z

[84] Serra G, Antona V, Cannata C, et al. Distal Arthrogryposis type 5 in an Italian family due to an autosomal dominant gain-of-function mutation of the PIEZO2 gene. Ital J Pediatr. 2022;48(1). DOI: 10.1186/s13052-022-01329-z

[85] Oliwa A, Hendson G, Longman C, et al. Lethal respiratory course and additional features expand the phenotypic spectrum of PIEZO2-related distal arthrogryposis type 5. Am J Med Genet A. 2022. DOI: 10.1002/ajmg.a.63019

[86] Oliwa A., Hendson G., Longman C., et al. Lethal respiratory course and additional features expand the phenotypic spectrum of PIEZO2-related distal arthrogryposis type 5 // Am. J. Med. Genet. A. 2023. Vol. 191. No. 2. P. 546–553. DOI: 10.1002/ajmg.a.63019

[87] Oliwa A, Hendson G, Longman C, et al. Lethal respiratory course and additional features expand the phenotypic spectrum of PIEZO2-related distal arthrogryposis type 5. Am J Med Genet A. 2022. DOI: 10.1002/ajmg.a.63019

[88] Dai S, Dieterich K, Jaeger M, et al. Disability in adults with arthrogryposis is severe, partly invisible, and varies by genotype. Neurology. 2018;90(18):e1596–e1604. DOI: 10.1212/WNL.0000000000005418

[89] Dai S., Dieterich K., Jaeger M., et al. Disability in adults with arthrogryposis is severe, partly invisible, and varies by genotype // Neurology. 2018. Vol. 90. No. 18. DOI: 10.1212/WNL.0000000000005418

[90] Dai S, Dieterich K, Jaeger M, et al. Disability in adults with arthrogryposis is severe, partly invisible, and varies by genotype. Neurology. 2018;90(18):e1596–e1604. DOI: 10.1212/WNL.0000000000005418

[91] Delle Vedove A, Storbeck M, Heller R, et al. Biallelic loss of proprioception-related PIEZO2 causes muscular atrophy with perinatal respiratory distress, arthrogryposis, and scoliosis. Am J Hum Genet. 2016;99(6):1406–1408. DOI: 10.1016/j.ajhg.2016.11.009

[92] Delle Vedove A., Storbeck M., Heller R., et al. Biallelic loss of proprioception-related PIEZO2 causes muscular atrophy with perinatal respiratory distress, arthrogryposis, and scoliosis // Am. J. Hum. Genet. 2016. Vol. 99. No. 6. P. 1406–1408. DOI: 10.1016/j.ajhg.2016.11.009

[93] Delle Vedove A, Storbeck M, Heller R, et al. Biallelic loss of proprioception-related PIEZO2 causes muscular atrophy with perinatal respiratory distress, arthrogryposis, and scoliosis. Am J Hum Genet. 2016;99(6):1406–1408. DOI: 10.1016/j.ajhg.2016.11.009

[94] Alper SL. Genetic diseases of PIEZO1 and PIEZO2 dysfunction. Curr Top Membr. 2017;79:97–134. DOI: 10.1016/bs.ctm.2017.01.001

[95] Alper S.L. Genetic diseases of PIEZO1 and PIEZO2 dysfunction // Curr. Top Membr. 2017. Vol. 79. No. 97–134. DOI: 10.1016/bs.ctm.2017.01.001

[96] Alper SL. Genetic diseases of PIEZO1 and PIEZO2 dysfunction. Curr Top Membr. 2017;79:97–134. DOI: 10.1016/bs.ctm.2017.01.001

[97] Chesler AT, Szczot M, Bharucha-Goebel D, et al. The role of PIEZO2 in human mechanosensation. N Engl J Med. 2016;375(14):1355–1364. DOI: 10.1056/NEJMoa1602812

[98] Chesler A.T., Szczot M., Bharucha-Goebel D., et al. The role of PIEZO2 in human mechanosensation // N. Engl. J. Med. 2016. Vol. 375. No. 14. P. 1355–1364. DOI: 10.1056/NEJMoa1602812

[99] Chesler AT, Szczot M, Bharucha-Goebel D, et al. The role of PIEZO2 in human mechanosensation. N Engl J Med. 2016;375(14):1355–1364. DOI: 10.1056/NEJMoa1602812

[100] Mahmud AA, Nahid NA, Nassif C, et al. Loss of the proprioception and touch sensation channel PIEZO2 in siblings with a progressive form of contractures. Clin Genet. 2017;91(3):470–475. DOI: 10.1111/cge.12850

[101] Mahmud A.A., Nahid N.A., Nassif C., et al. Loss of the proprioception and touch sensation channel PIEZO2 in siblings with a progressive form of contractures // Clin. Genet. 2017. Vol. 91. No. 3. P. 470–475. DOI: 10.1111/cge.12850

[102] Mahmud AA, Nahid NA, Nassif C, et al. Loss of the proprioception and touch sensation channel PIEZO2 in siblings with a progressive form of contractures. Clin Genet. 2017;91(3):470–475. DOI: 10.1111/cge.12850

[103] Haliloglu G, Becker K, Temucin C, et al. Recessive PIEZO2 stop mutation causes distal arthrogryposis with distal muscle weakness, scoliosis and proprioception defects. J Hum Genet. 2017;62(4):497–501. DOI: 10.1038/jhg.2016.153

[104] Haliloglu G., Becker K., Temucin C., et al. Recessive PIEZO2 stop mutation causes distal arthrogryposis with distal muscle weakness, scoliosis and proprioception defects // J. Hum. Genet. 2017. Vol. 62. No. 4. P. 497–501. DOI: 10.1038/jhg.2016.153

[105] Haliloglu G, Becker K, Temucin C, et al. Recessive PIEZO2 stop mutation causes distal arthrogryposis with distal muscle weakness, scoliosis and proprioception defects. J Hum Genet. 2017;62(4):497–501. DOI: 10.1038/jhg.2016.153

[106] Behunova J, GerykovaBujalkova M, Gras G, et al. Distal arthrogryposis with impaired proprioception and touch: description of an early phenotype in a boy with compound heterozygosity of PIEZO2 mutations and review of the literature. Mol Syndromol. 2019;9(6):287–294. DOI: 10.1159/000494451

[107] Behunova J., GerykovaBujalkova M., Gras G., et al. Distal arthrogryposis with impaired proprioception and touch: description of an early phenotype in a boy with compound heterozygosity of PIEZO2 mutations and review of the literature // Mol. Syndromol. 2019. Vol. 9. No. 6. P. 287–294. DOI: 10.1159/000494451

[108] Behunova J, GerykovaBujalkova M, Gras G, et al. Distal arthrogryposis with impaired proprioception and touch: description of an early phenotype in a boy with compound heterozygosity of PIEZO2 mutations and review of the literature. Mol Syndromol. 2019;9(6):287–294. DOI: 10.1159/000494451

[109] Yamaguchi T, Takano K, Inaba Y, et al. PIEZO2 deficiency is a recognizable arthrogryposis syndrome: a new case and literature review. Am J Med Genet A. 2019;179(6):948–957. DOI: 10.1002/ajmg.a.61142

[110] Yamaguchi T., Takano K., Inaba Y., et al. PIEZO2 deficiency is a recognizable arthrogryposis syndrome: a new case and literature review // Am. J. Med. Genet. A. 2019. Vol. 179. No. 6. P. 948–957. DOI: 10.1002/ajmg.a.61142

[111] Yamaguchi T, Takano K, Inaba Y, et al. PIEZO2 deficiency is a recognizable arthrogryposis syndrome: a new case and literature review. Am J Med Genet A. 2019;179(6):948–957. DOI: 10.1002/ajmg.a.61142

[112] Oakley-Hannibal E, Ghali N, Pope FM, et al. A neuromuscular disorder with homozygosity for PIEZO2 gene variants: an important differential diagnosis for kyphoscoliotic Ehlers-Danlos syndrome. Clin Dysmorphol. 2020;29(1):69–72. DOI: 10.1097/MCD.0000000000000304

[113] Oakley-Hannibal E., Ghali N., Pope F.M., et al. A neuromuscular disorder with homozygosity for PIEZO2 gene variants: an important differential diagnosis for kyphoscoliotic Ehlers-Danlos syndrome // Clin. Dysmorphol. 2020. Vol. 29. No. 1. P. 69–72. DOI: 10.1097/MCD.0000000000000304

[114] Oakley-Hannibal E, Ghali N, Pope FM, et al. A neuromuscular disorder with homozygosity for PIEZO2 gene variants: an important differential diagnosis for kyphoscoliotic Ehlers-Danlos syndrome. Clin Dysmorphol. 2020;29(1):69–72. DOI: 10.1097/MCD.0000000000000304

[115] Klaniewska M, Jedrzejowska M, Rydzanicz M, et al. Case report: further delineation of neurological symptoms in young children caused by compound heterozygous mutation in the PIEZO2 gene. Front Genet. 2021;12. DOI: 10.3389/fgene.2021.620752

[116] Klaniewska M., Jedrzejowska M., Rydzanicz M., et al. Case report: further delineation of neurological symptoms in young children caused by compound heterozygous mutation in the PIEZO2 gene // Front. Genet. 2021. Vol. 12. DOI: 10.3389/fgene.2021.620752

[117] Klaniewska M, Jedrzejowska M, Rydzanicz M, et al. Case report: further delineation of neurological symptoms in young children caused by compound heterozygous mutation in the PIEZO2 gene. Front Genet. 2021;12. DOI: 10.3389/fgene.2021.620752

[118] Markova TV, Dadali EL, Nikitin SS, et al. Clinical and genetic characteristics of distal arthrogryposis caused by mutations in the PIEZO2 gene. Neuromuscular Diseases. 2021;11(2):48–55. (In Russ.) DOI: 10.17650/2222-8721-2021-11-2-48-55

[119] Маркова Т.В., Дадали Е.Л., Никитин С.С., и др. Клинико-генетические характеристики дистальных артрогрипозов, обусловленных мутациями в гене PIEZO2 // Нервно-мышечные болезни 2021. Т. 11. № 2. С. 48–55. DOI: 10.17650/2222-8721-2021-11-2-48-55

[120] Markova TV, Dadali EL, Nikitin SS, et al. Clinical and genetic characteristics of distal arthrogryposis caused by mutations in the PIEZO2 gene. Neuromuscular Diseases. 2021;11(2):48–55. (In Russ.) DOI: 10.17650/2222-8721-2021-11-2-48-55

Funding

Государственное задание Минздрава России(НИР № 121031700125-7)

RIGHTS & PERMISSIONS

Chernyavskaya-Haukka V.V., Agranovich O.E.