Stem cell niches and endogenous electric fields in tissue repair

Abstract

Adult stem cells are responsible for homeostasis and repair of many tissues. Endogenous adult stem cells reside in certain regions of organs, known as the stem cell niche, which is recognized to have an important role in regulating tissue maintenance and repair. In wound healing and tissue repair, stem cells are mobilized and recruited to the site of wound, and participate in the repair process. Many regulatory factors are involved in the stem cell-based repair process, including stem cell niches and endogenous wound electric fields, which are present at wound tissues and proved to be important in guiding wound healing. Here we briefly review the role of stem cell niches and endogenous electric fields in tissue repair, and hypothesize that endogenous electric fields become part of stem cell niche in the wound site.

Key words： stem cell; stem cell niche; electric field; tissue repair

Acknowledgements

We are very grateful to Professor Min Zhao (University of California, Davis) for his great help of critical reading of the manuscript. This work is supported by Key Program of National Nature Science Foundation of China (81030037) and Open fund of State Key Laboratory of Trauma, Burns and Combined Injury, Third Military Medical University (SKLZZ200804).

References

1 Doetsch F. A niche for adult neural stem cells. Curr Opin Genet Dev, 2003, 13(5): 543–550

PMID

2 Nuccitelli R. A role for endogenous electric fields in wound healing. Curr Top Dev Biol, 2003, 58: 1–26

PMID

3 Zhao M, Song B, Pu J, Wada T, Reid B, Tai G, Wang F, Guo A, Walczysko P, Gu Y, Sasaki T, Suzuki A, Forrester J V, Bourne H R, Devreotes P N, McCaig C D, Penninger J M. Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature, 2006, 442(7101): 457–460

PMID

4 Scadden D T. The stem-cell niche as an entity of action. Nature, 2006, 441(7097): 1075–1079

PMID

5 Jones D L, Wagers A J. No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol, 2008, 9(1): 11–21

PMID

6 Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell, 2004, 116(6): 769–778

PMID

7 Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells, 1978, 4(1-2): 7–25

PMID

8 Nie D. Cancer stem cell and niche. Front Biosci (Schol Ed), 2010, 2(1): 184–193 (Schol Ed)

PMID

9 King F J, Lin H. Somatic signaling mediated by fs(1)Yb is essential for germline stem cell maintenance during Drosophila oogenesis. Development, 1999, 126(9): 1833–1844

PMID

10 Xie T, Spradling A C. A niche maintaining germ line stem cells in the Drosophila ovary. Science, 2000, 290(5490): 328–330

PMID

11 Tumbar T, Guasch G, Greco V, Blanpain C, Lowry W E, Rendl M, Fuchs E. Defining the epithelial stem cell niche in skin. Science, 2004, 303(5656): 359–363

PMID

12 Yen T H, Wright N A. The gastrointestinal tract stem cell niche. Stem Cell Rev, 2006, 2(3): 203–212

PMID

13 Conover J C, Notti R Q. The neural stem cell niche. Cell Tissue Res, 2008, 331(1): 211–224

PMID

14 Mitsiadis T A, Barrandon O, Rochat A, Barrandon Y, De Bari C. Stem cell niches in mammals. Exp Cell Res, 2007, 313(16): 3377–3385

PMID

15 Ohshima H, Nakasone N, Hashimoto E, Sakai H, Nakakura-Ohshima K, Harada H. The eternal tooth germ is formed at the apical end of continuously growing teeth. Arch Oral Biol, 2005, 50(2): 153–157

PMID

16 Wilson A, Trumpp A. Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol, 2006, 6(2): 93–106

PMID

17 Mohyeldin A, Garzón-Muvdi T, Quiñones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell, 2010, 7(2): 150–161

PMID

18 Moore K A, Lemischka I R. Stem cells and their niches. Science, 2006, 311(5769): 1880–1885

PMID

19 Alonso L, Fuchs E. Stem cells of the skin epithelium. Proc Natl Acad Sci USA, 2003, 100(90001 Suppl 1): 11830–11835

PMID

20 Morris R J, Liu Y, Marles L, Yang Z, Trempus C, Li S, Lin J S, Sawicki J A, Cotsarelis G. Capturing and profiling adult hair follicle stem cells. Nat Biotechnol, 2004, 22(4): 411–417

PMID

21 Morris R J, Potten C S. Slowly cycling (label-retaining) epidermal cells behave like clonogenic stem cells in vitro. Cell Prolif, 1994, 27(5): 279–289

PMID

22 Cotsarelis G, Sun T T, Lavker R M. Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell, 1990, 61(7): 1329–1337

PMID

23 Luo J, Daniels S B, Lennington J B, Notti R Q, Conover J C. The aging neurogenic subventricular zone. Aging Cell, 2006, 5(2): 139–152

PMID

24 Luskin M B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron, 1993, 11(1): 173–189

PMID

25 Menn B, Garcia-Verdugo J M, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci, 2006, 26(30): 7907–7918

PMID

26 Seri B, García-Verdugo J M, Collado-Morente L, McEwen B S, Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol, 2004, 478(4): 359–378

PMID

27 Park H C, Yasuda K, Kuo M C, Ni J, Ratliff B B, Chander P N, Goligorsky M S. Renal capsule as a stem cell niche. Am J Physiol Renal Physiol, 2010, 67(5): 1254–1262

PMID

28 Kim K, Lee K M, Han D J, Yu E, Cho Y M. Adult stem cell-like tubular cells reside in the corticomedullary junction of the kidney. Int J Clin Exp Pathol, 2008, 1(3): 232–241

PMID

29 Bearzi C, Rota M, Hosoda T, Tillmanns J, Nascimbene A, De Angelis A, Yasuzawa-Amano S, Trofimova I, Siggins R W, Lecapitaine N, Cascapera S, Beltrami A P, D’Alessandro D A, Zias E, Quaini F, Urbanek K, Michler R E, Bolli R, Kajstura J, Leri A, Anversa P. Human cardiac stem cells. Proc Natl Acad Sci USA, 2007, 104(35): 14068–14073

PMID

30 Urbanek K, Cesselli D, Rota M, Nascimbene A, De Angelis A, Hosoda T, Bearzi C, Boni A, Bolli R, Kajstura J, Anversa P, Leri A. Stem cell niches in the adult mouse heart. Proc Natl Acad Sci USA, 2006, 103(24): 9226–9231

PMID

31 Zhang J, Niu C, Ye L, Huang H, He X, Tong W G, Ross J, Haug J, Johnson T, Feng J Q, Harris S, Wiedemann L M, Mishina Y, Li L. Identification of the haematopoietic stem cell niche and control of the niche size. Nature, 2003, 425(6960): 836–841

PMID

32 Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, Ito K, Koh G Y, Suda T. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell, 2004, 118(2): 149–161

PMID

33 Kiel M J, Yilmaz O H, Iwashita T, Yilmaz O H, Terhorst C, Morrison S J. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell, 2005, 121(7): 1109–1121

PMID

34 Kopp H G, Avecilla S T, Hooper A T, Rafii S. The bone marrow vascular niche: home of HSC differentiation and mobilization. Physiology (Bethesda), 2005, 20(5): 349–356

PMID

35 Zhang J, Li L. Stem cell niche: microenvironment and beyond. J Biol Chem, 2008, 283(15): 9499–9503

PMID

36 Barker A T, Jaffe L F, Vanable J W Jr. The glabrous epidermis of cavies contains a powerful battery. Am J Physiol, 1982, 242(3): R358–R366

PMID

37 Candia O A. Electrolyte and fluid transport across corneal, conjunctival and lens epithelia. Exp Eye Res, 2004, 78(3): 527–535

PMID

38 Mukerjee E V, Isseroff R R, Nuccitelli R, Collins S D, Smith R L. Microneedle array for measuring wound generated electric fields. Conf Proc IEEE Eng Med Biol Soc, 2006, 1: 4326–4328

PMID

39 Nuccitelli R, Nuccitelli P, Ramlatchan S, Sanger R, Smith P J. Imaging the electric field associated with mouse and human skin wounds. Wound Repair Regen, 2008, 16(3): 432–441

PMID

40 McCaig C D, Rajnicek A M, Song B, Zhao M. Controlling cell behavior electrically: current views and future potential. Physiol Rev, 2005, 85(3): 943–978

PMID

41 Zhao M. Electrical fields in wound healing-An overriding signal that directs cell migration. Semin Cell Dev Biol, 2009, 20(6): 674–682

PMID

42 Song B, Zhao M, Forrester J V, McCaig C D. Electrical cues regulate the orientation and frequency of cell division and the rate of wound healing in vivo. Proc Natl Acad Sci USA, 2002, 99(21): 13577–13582

PMID

43 Arocena M, Zhao M, Collinson J M, Song B. A time-lapse and quantitative modelling analysis of neural stem cell motion in the absence of directional cues and in electric fields. J Neurosci Res, 2010, 88(15): 3267–3274

PMID

44 Ariza C A, Fleury A T, Tormos C J, Petruk V, Chawla S, Oh J, Sakaguchi D S, Mallapragada S K. The influence of electric fields on hippocampal neural progenitor cells. Stem Cell Rev, 2010, 6(4): 585–600

PMID

45 Hammerick K E, Longaker M T, Prinz F B. In vitro effects of direct current electric fields on adipose-derived stromal cells. Biochem Biophys Res Commun, 2010, 397(1): 12–17

PMID

46 Sun S, Titushkin I, Cho M. Regulation of mesenchymal stem cell adhesion and orientation in 3D collagen scaffold by electrical stimulus. Bioelectrochemistry, 2006, 69(2): 133–141

PMID

47 Tandon N, Goh B, Marsano A, Chao P H, Montouri-Sorrentino C, Gimble J, Vunjak-Novakovic G. Alignment and elongation of human adipose-derived stem cells in response to direct-current electrical stimulation. Conf Proc IEEE Eng Med Biol Soc, 2009, 2009(1): 6517–6521

PMID

48 Serena E, Figallo E, Tandon N, Cannizzaro C, Gerecht S, Elvassore N, Vunjak-Novakovic G. Electrical stimulation of human embryonic stem cells: cardiac differentiation and the generation of reactive oxygen species. Exp Cell Res, 2009, 315(20): 3611–3619

PMID