A critical size volumetric muscle loss model in mouse masseter with impaired mastication on nutrition

Abstract

Orofacial muscle defect due to congenital anomalies, tumour ablation or traumatic accident that exceeds endogenous regeneration capacity may lead to sustained deficits in masticatory function and nutrition intake. Functional recovery has always been the goal of muscle tissue repair, but currently, there is no suitable model for quantitative analyses of either functional consequences or treatment efficacy of orofacial muscle defect. This study proposed a critical size volumetric muscle loss (VML) model in mouse masseter with impaired mastication on nutrition. Full-thickness VML defects in diameter of 1.0, 1.5, 2.0 and 3.0 mm were generated in the centre of the mouse masseter using a biopsy punch to determine the critical size for functional impairment. In the VML region, myogenesis was dampened but fibrogenesis was activated, as long with a reduction in the density of the neuromuscular junction and an increase in vascular density. Accordingly, persistent fibrosis was observed in the centre region of VML in all diameters. The 2.0 mm diameter was the critical threshold to masticatory function impairment after VML in the masseter. VML of 3.0 mm diameter led to a significant impact on nutrition intake and body weight gain. Autologous muscle graft effectively relieved the fibrosis and functional deficit after VML injury in the masseter. This model serves as a reliable tool in studying functional recovery strategies for orofacial muscle defects.

References

1 Gilbert-Honick J, Grayson W. Vascularized and innervated skeletal muscle tissue engineering. Adv Healthc Mater. 2020;9(1):e1900626.

2 Dumont NA, Bentzinger CF, Sincennes MC, Rudnicki MA. Satellite cells and skeletal muscle regeneration. Compr Physiol. 2015;5(3):1027-1059.

3 Corona BT, Wenke JC, Ward CL. Pathophysiology of volumetric muscle loss injury. Cells Tissues Organs. 2016;202(3–4):180-188.

4 Vega-Soto EE, Rodriguez BL, Armstrong RE, Larkin LM. A 30% volumetric muscle loss does not result in sustained functional deficits after a 90-day recovery in rats. Regen Eng Transl Med. 2020;6(1):62-68.

5 Eugenis I, Wu D, Rando TA. Cells, scaffolds, and bioactive factors: engineering strategies for improving regeneration following volumetric muscle loss. Biomaterials. 2021;278:121173.

6 Jin Y, Shahriari D, Jeon EJ, et al. Functional skeletal muscle regeneration with thermally drawn porous fibers and reprogrammed muscle progenitors for volumetric muscle injury. Adv Mater. 2021;33(14):e2007946.

7 Kim H, Kwon YT, Zhu C, et al. Real-time functional assay of volumetric muscle loss injured mouse masseter muscles via nanomembrane electronics. Adv Sci (Weinh). 2021;8(17):e2101037.

8 Noden DM, Francis-West P. The differentiation and morphogenesis of craniofacial muscles. Dev Dyn. 2006;235(5):1194-1218.

9 Cheng X, Huang H, Luo X, Shi B, Li J. Wnt7a induces satellite cell expansion, myofiber hyperplasia and hypertrophy in rat craniofacial muscle. Sci Rep. 2018;8(1):10613.

10 Mootoosamy RC, Dietrich S. Distinct regulatory cascades for head and trunk myogenesis. Development. 2002;129(3):573-583.

11 Rosero Salazar DH, Carvajal Monroy PL, Wagener FADTG, Von den Hoff JW. Orofacial muscles: embryonic development and regeneration after injury. J Dent Res. 2020;99(2):125-132.

12 Cheng X, Huang Y, Liu Y, et al. Head muscle fibro-adipogenic progenitors account for the tilted regeneration towards fibrosis. Biochem Biophys Res Commun. 2022;589:131-138.

13 Pavlath GK, Thaloor D, Rando TA, Cheong M, English AW, Zheng B. Heterogeneity among muscle precursor cells in adult skeletal muscles with differing regenerative capacities. Dev Dyn. 1998;212(4):495-508.

14 Ono Y, Boldrin L, Knopp P, Morgan JE, Zammit PS. Muscle satellite cells are a functionally heterogeneous population in both somite-derived and branchiomeric muscles. Dev Biol. 2010;337(1):29-41.

15 Sicari BM, Agrawal V, Siu BF, et al. A murine model of volumetric muscle loss and a regenerative medicine approach for tissue replacement. Tissue Eng Part A. 2012;18(19–20):1941-1948.

16 Wu X, Corona BT, Chen X, Walters TJ. A standardized rat model of volumetric muscle loss injury for the development of tissue engineering therapies. Biores Open Access. 2012;1(6):280-290.

17 Corona BT, Henderson BE, Ward CL, Greising SM. Contribution of minced muscle graft progenitor cells to muscle fibre formation after volumetric muscle loss injury in wild-type and immune deficient mice. Physiol Rep. 2017;5(7):e13249.

18 Anderson SE, Han WM, Srinivasa V, et al. Determination of a critical size threshold for volumetric muscle loss in the mouse quadriceps. Tissue Eng Part C Methods. 2019;25(2):59-70.

19 Lever TE, Gorsek A, Cox KT, et al. An animal model of oral dysphagia in amyotrophic lateral sclerosis. Dysphagia. 2009;24(2):180-195.

20 Freeman PW, Lemen CA. Measuring bite force in small mammals with a piezo-resistive sensor. J Mammal. 2008;89:513-517.

21 Grippo RM, Tang Q, Zhang Q, et al. Dopamine signaling in the Suprachiasmatic nucleus enables weight gain associated with hedonic feeding. Curr Biol. 2020;30(2):196-208.

22 Stern SA, Azevedo EP, Pomeranz LE, Doerig KR, Ivan VJ, Friedman JM. Top down control of conditioned overconsumption is mediated by insular cortex Nos1 neurons. Cell Metab. 2021;33(7):1418-1432.

23 Pétrault M, Ouk T, Bastide M, Bordet R, Pétrault O, Bérézowski V. Age and diet modify acute microhemorrhage outcome in the mouse brain. Neurobiol Aging. 2021;98:99-107.

24 Kacířová M, Železná B, Blažková M, et al. Aging and high-fat diet feeding lead to peripheral insulin resistance and sex-dependent changes in brain of mouse model of tau pathology THY-Tau22. J Neuroinflammation. 2021;18(1):141.

25 Henderson YO, Bithi N, Link C, et al. Late-life intermittent fasting decreases aging-related frailty and increases renal hydrogen sulfide production in a sexually dimorphic manner. Geroscience. 2021;43(4):1527-1554.

26 Cohen IL, Gardner JM, Karmel BZ, Kim SY. Rating scale measures are associated with Noldus EthoVision-XT video tracking of behaviors of children on the autism spectrum. Mol Autism. 2014;5(1):15.

27 Cox PG, Jeffery N. Reviewing the morphology of the jaw-closing musculature in squirrels, rats, and Guinea pigs with contrast-enhanced microCT. Anat Rec (Hoboken). 2011;294(6):915-928.

28 Kankala RK, Zhao J, Liu CG, et al. Highly porous microcarriers for minimally invasive in situ skeletal muscle cell delivery. Small. 2019;15(25):e1901397.

29 Quarta M, Cromie M, Chacon R, et al. Bioengineered constructs combined with exercise enhance stem cell-mediated treatment of volumetric muscle loss. Nat Commun. 2017;8:15613.

30 Cheng X, Shi B, Li J. Distinct embryonic origin and injury response of resident stem cells in craniofacial muscles. Front Physiol. 2021;12:690248.

31 Randolph ME, Phillips BL, Choo HJ, Vest KE, Vera Y, Pavlath GK. Pharyngeal satellite cells undergo Myogenesis under basal conditions and are required for pharyngeal muscle maintenance. Stem Cells. 2015;33(12):3581-3595.

32 Keefe AC, Lawson JA, Flygare SD, et al. Muscle stem cells contribute to myofibres in sedentary adult mice. Nat Commun. 2015;6:7087.

33 Park JS, Jung YJ, Kim MJ. Effects of neuromuscular electrical stimulation synchronized with chewing exercises on bite force and masseter muscle thickness in community-dwelling older adults in South Korea: a randomized controlled trial. Int J Environ Res Public Health. 2020;17(13):4902.

34 Shiau YY, Peng CC, Hsu CW. Evaluation of biting performance with standardized test-foods. J Oral Rehabil. 1999;26(5):447-452.

35 Raadsheer MC, van Eijden TM, van Ginkel FC, Prahl-Andersen B. Contribution of jaw muscle size and craniofacial morphology to human bite force magnitude. J Dent Res. 1999;78(1):31-42.

36 Okayasu I, Yamada Y, Kohno S, Yoshida N. New animal model for studying mastication in oral motor disorders. J Dent Res. 2003;82(4):318-321.

37 Kobayashi M, Masuda Y, Fujimoto Y, et al. Electrophysiological analysis of rhythmic jaw movements in the freely moving mouse. Physiol Behav. 2002;75(3):377-385.

38 Hiiemae KM, Palmer JB. Food transport and bolus formation during complete feeding sequences on foods of different initial consistency. Dysphagia. 1999;14(1):31-42.

39 Williams SH, Peiffer E, Ford S. Gape and bite force in the rodents Onychomys leucogaster and Peromyscus maniculatus: does jaw-muscle anatomy predict performance?J Morphol. 2009;270(11):1338-1347.

40 Chen Y, Williams SH, McNulty AL, et al. Temporomandibular joint pain: a critical role for Trpv4 in the trigeminal ganglion. Pain. 2013;154(8):1295-1304.

41 Kim SH, Son CN, Lee HJ, et al. Infliximab partially alleviates the bite force reduction in a mouse model of temporomandibular joint pain. J Korean Med Sci. 2015;30(5):552-558.

42 Huang E, Kang S, Park H, Park S, Ji Y, Holzapfel WH. Differences in anxiety levels of various murine models in relation to the gut microbiota composition. Biomedicine. 2018;6(4):113.

43 Diernberger S, Bernhardt O, Schwahn C, Kordass B. Self-reported chewing side preference and its associations with occlusal, temporomandibular and prosthodontic factors: results from the population-based Study of Health in Pomerania (SHIP-0). J Oral Rehabil. 2008;35(8):613-620.

44 Wilding RJ, Lewin A. A model for optimum functional human jaw movements based on values associated with preferred chewing patterns. Arch Oral Biol. 1991;36(7):519-523.

45 Santana-Mora U, López-Cedrún J, Mora MJ, Otero XL, Santana-Penín U. Temporomandibular disorders: the habitual chewing side syndrome. PloS One. 2013;8(4):e59980.

46 Poikela A, Kantomaa T, Pirttiniemi P. Craniofacial growth after a period of unilateral masticatory function in young rabbits. Eur J Oral Sci. 1997;105(4):331-337.

47 Poikela A, Kantomaa T, Pirttiniemi P, Tuukkanen J, Pietilä K. Unilateral masticatory function changes the proteoglycan content of mandibular condylar cartilage in rabbit. Cells Tissues Organs. 2000;167(1):49-57.

48 Wu M, Wang X, Shuai J, et al. Identification of key miRNAs in unilateral mastication-induced disruption of cartilage homeostasis. Oral Dis. 2023.

49 Liu Z, Hou Y, Zhang P, Lu H, Wang W, Ma W. Changes of the condylar cartilage and subchondral bone in the temporomandibular joints of rats under unilateral mastication and expression of insulin-like growth Factor-1. J Stomatol Oral Maxillofac Surg. 2022;123(4):405-416.

50 Ju YM, Atala A, Yoo JJ, Lee SJ. In situ regeneration of skeletal muscle tissue through host cell recruitment. Acta Biomater. 2014;10(10):4332-4339.

51 Eugenis I, Wu D, Hu C, Chiang G, Huang NF, Rando TA. Scalable macroporous hydrogels enhance stem cell treatment of volumetric muscle loss. Biomaterials. 2022;290:121818.

52 Zhang Z, Zhao X, Wang C, Huang Y, Han Y, Guo B. Injectable conductive micro-cryogel as a muscle stem cell carrier improves myogenic proliferation, differentiation and in situ skeletal muscle regeneration. Acta Biomater. 2022;151:197-209.