Macrophage-stimulating protein promotes hair growth ex vivo and induces anagen from telogen stage hair follicles in vivo

Journal of Investigative Dermatology

Volumn 123, Issue 1, 2004, Pages 34-40

  McElwee, Kevin J ^a   Huth, Andrea ^a   Kissling, Sabine ^a   Hoffmann, Rolf ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Growth factor; Hepatocyte growth factor like protein; Macrophage stimulating protein receptor

Indexed keywords

AGAROSE; MACROPHAGE ACTIVATING FACTOR; SCATTER FACTOR;

ARTICLE; CELL GROWTH; CELL MATURATION; CONTROLLED STUDY; HAIR FOLLICLE; HAIR GROWTH; HAIR ROOT; HUMAN; HUMAN TISSUE; IMMUNOHISTOLOGY; INCUBATION TIME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; SWEAT GLAND; WESTERN BLOTTING;

EID: 3042686851     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0022-202X.2004.22712.x     Document Type: Article

References (48)

1. Bezerra JA, Carrick TL, Degen JL, Witte D, Degen SJ: Biological effects of targeted inactivation of hepatocyte growth factor-like protein in mice. J Clin Invest 101:1175-1183, 1998
2. Botchkarev VA, Botchkareva NV, Nakamura M, et al: Noggin is required for induction of the hair follicle growth phase in postnatal skin. FASEB J 15:2205-2214, 2001
3. Chuong CM, Hou L, Chen PJ, Wu P, Patel N, Chen Y: Dinosaur's feather and chicken's tooth? Tissue engineering of the integument. Eur J Dermatol 11:286-292, 2001
4. Chuong CM, Widelitz RB, Ting-Berreth S, Jiang TX: Early events during avian skin appendage regeneration: Dependence on epithelial-mesenchymal interaction and order of molecular reappearance. J Invest Dermatol 107:639-646, 1996
5. Cowin AJ, Kallincos N, Hatzirodos N, Robertson JG, Pickering KJ, Couper J, Belford DA: Hepatocyte growth factor and macrophage-stimulating protein are upregulated during excisional wound repair in rats. Cell Tissue Res 306:239-250, 2001
6. Danilkovitch A, Donley S, Skeel A, Leonard EJ: Two independent signaling pathways mediate the antiapoptotic action of macrophage-stimulating protein on epithelial cells. Mol Cell Biol 20:2218-2227, 2000
7. Danilkovitch-Miagkova A, Leonard EJ: Anti-apoptotic action of macrophage stimulating protein (MSP). Apoptosis 6:183-190, 2001
8. Danilkovitch-Miagkova A, Miagkov A, Skeel A, Nakaigawa N, Zbar B, Leonard EJ: Oncogenic mutants of RON and MET receptor tyrosine kinases cause activation of the beta-catenin pathway. Mol Cell Biol 21:5857-5868, 2001
9. Dry FW: The coat of the mouse (Mus Musculus). J Genet 16:287-340, 1926
10. Eicheler W, Happle R, Hoffmann R: 5 alpha-reductase activity in the human hair follicle concentrates in the dermal papilla. Arch Dermatol Res 290:126-132, 1998
11. Funakoshi H, Nakamura T: Identification of HGF-like protein as a novel neurotrophic factor for avian dorsal root ganglion sensory neurons. Biochem Biophys Res Commun 283:606-612, 2001
12. Gat U, DasGupta R, Degenstein L, Fuchs E: De Novo hair follicle morphogenesis and hair tumors in mice expressing a truncated beta-catenin in skin. Cell 95:605-614, 1998
13. Gaudino G, Avantaggiato V, Follenzi A, Acampora D, Simeone A, Comoglio PM: The proto-oncogene RON is involved in development of epithelial, bone and neuro-endocrine tissues. Oncogene 11:2627-2637, 1995
14. Gaudino G, Follenzi A, Naldini L, et al: RON is a heterodimeric tyrosine kinase receptor activated by the HGF homologue MSP. EMBO J 13:3524-3532, 1994
15. Iwama A, Wang MH, Yamaguchi N, et al: Terminal differentiation of murine resident peritoneal macrophages is characterized by expression of the STK protein tyrosine kinase, a receptor for macrophage-stimulating protein. Blood 86:3394-3403, 1995
16. Jindo T, Imai R, Tsuboi R, Takamori K, Ogawa H: The effect of various cytokines on hair growth of mouse vibrissae in organ culture. J Dermatol Sci 7:S73-S78, 1994
17. Jindo T, Tsuboi R, Imai R, Takamori K, Rubin JS, Ogawa H: The effect of hepatocyte growth factor/scatter factor on human hair follicle growth. J Dermatol Sci 10:229-232, 1995
18. Jindo T, Tsuboi R, Takamori K, Ogawa H: Local injection of hepatocyte growth factor/scatter factor (HGF/SF) alters cyclic growth of murine hair follicles. J Invest Dermatol 110:338-342, 1998
19. Kurihara N, Iwama A, Tatsumi J, Ikeda K, Suda T: Macrophage-stimulating protein activates STK receptor tyrosine kinase on osteoclasts and facilitates bone resorption by osteoclast-like cells. Blood 87:3704-3710, 1996
20. Kurihara N, Tatsumi J, Arai F, Iwama A, Suda T: Macrophage-stimulating protein (MSP) and its receptor, RON, stimulate human osteoclast activity but not proliferation: Effect of MSP distinct from that of hepatocyte growth factor. Exp Hematol 26:1080-1085, 1998
21. Leonard EJ: Biological aspects of macrophage-stimulating protein (MSP) and its receptor. Ciba Found Symp 212:183-197, 1997
22. Leonard EJ, Skeel A: A serum protein that stimulates macrophage movement, chemotaxis and spreading. Exp Cell Res 102:434-438, 1976
23. Leonard EJ, Skeel AH: Enhancement of spreading, phagocytosis and chemotaxis by macrophage stimulating protein (MSP). Adv Exp Med Biol 121B:181-194, 1979
24. Lindner G, Menrad A, Gherardi E, et al: Involvement of hepatocyte growth factor/scatter factor and met receptor signaling in hair follicle morphogenesis and cycling. FASEB J 14:319-332, 2000
25. McElwee K, Hoffmann R: Growth factors in early hair follicle morphogenesis. Eur J Dermatol 10:341-350, 2000
26. Medico E, Mongiovi AM, Huff J, et al: The tyrosine kinase receptors Ron and Sea control "scattering" and morphogenesis of liver progenitor cells in vitro. Mol Biol Cell 7:495-504, 1996
27. Muraoka RS, Sun WY, Colbert MC, Waltz SE, Witte DP, Degen JL, Friezner Degen SJ: The Ron/STK receptor tyrosine kinase is essential for peri-implantation development in the mouse. J Clin Invest 103:1277-1285, 1999
28. Nanney LB, Skeel A, Luan J, Polis S, Richmond A, Wang MH, Leonard EJ: Proteolytic cleavage and activation of pro-macrophage-stimulating protein and upregulation of its receptor in tissue injury. J Invest Dermatol 111:573-581, 1998
29. Quantin B, Schuhbaur B, Gesnel MC, Doll'e P, Breathnach R: Restricted expression of the ron gene encoding the macrophage stimulating protein receptor during mouse development. Dev Dyn 204:383-390, 1995
30. Relyea MJ, Miller J, Boggess D, Sundberg JP: Necropsy methods for laboratory mice: Biological characterization of a new mutation. In: Sundberg JP, Boggess D (eds). Systematic Approach to Evaluation of Mouse Mutations. Boca Raton, FL: CRC Press, 1999; p 57-90
31. Ronsin C, Muscatelli F, Mattei MG, Breathnach R: A novel putative receptor protein tyrosine kinase of the met family. Oncogene 8:1195-1202, 1993
32. Sakamoto O, Iwama A, Amitani R, et al: Role of macrophage-stimulating protein and its receptor, RON tyrosine kinase, in ciliary motility. J Clin Invest 99:701-709, 1997
33. Sengel P: Epidermal-dermal interactions during formation of skin and cutaneous appendages. In: Goldsmith LA (ed). Biochemistry and Physiology of the Skin, Vol. 1. New York: Oxford University Press, 1983; p 102-131
34. Shimaoka S, Tsuboi R, Jindo T, Imai R, Takamori K, Rubin JS, Ogawa H: Hepatocyte growth factor/scatter factor expressed in follicular papilla cells stimulates human hair growth in vitro. J Cell Physiol 165:333-338, 1995
35. Skeel A, Yoshimura T, Showalter SD, Tanaka S, Appella E, Leonard EJ: Macrophage stimulating protein: Purification, partial amino acid sequence, and cellular activity. J Exp Med 173:1227-1234, 1991
36. Sonnenberg E, Meyer D, Weidner KM, Birchmeier C: Scatter factor/hepatocyte growth factor and its receptor, the c-met tyrosine kinase, can mediate a signal exchange between mesenchyme and epithelia during mouse development. J Cell Biol 123:223-235, 1993
37. Stella MC, Vercelli A, Repici M, Follenzi A, Comoglio PM: Macrophage stimulating protein is a novel neurotrophic factor. Mol Biol Cell 12:1341-1352, 2001
38. Tamagnone L, Comoglio PM: Control of invasive growth by hepatocyte growth factor (HGF) and related scatter factors. Cytokine Growth Factor Rev 8:129-142, 1997
39. Thery C, Sharpe MJ, Batley SJ, Stern CD, Gherardi E: Expression of HGF/SF, HGF1/MSP, and c-met suggests new functions during early chick development. Dev Genet 17:90-101, 1995
40. Wang MH, Dlugosz AA, Sun Y, Suda T, Skeel A, Leonard EJ: Macrophage-stimulating protein induces proliferation and migration of murine keratinocytes. Exp Cell Res 226:39-46, 1996a
41. Wang MH, Gonias SL, Skeel A, Wolf BB, Yoshimura T, Leonard EJ: Proteolytic activation of single-chain precursor macrophage-stimulating protein by nerve growth factor-gamma and epidermal growth factor-binding protein, members of the kallikrein family. J Biol Chem 269:13806-13810, 1994a
42. Wang MH, Iwama A, Skeel A, Suda T, Leonard EJ: The murine stk gene product, a transmembrane protein tyrosine kinase, is a receptor for macrophage-stimulating protein. Proc Natl Acad Sci USA 92:3933-3937, 1995
43. Wang MH, Julian FM, Breathnach R, et al: Macrophage stimulating protein (MSP) binds to its receptor via the MSP beta chain. J Biol Chem 272:16999-17004, 1997
44. Wang MH, Ronsin C, Gesnel MC, Coupey L, Skeel A, Leonard EJ, Breathnach R: Identification of the ron gene product as the receptor for the human macrophage stimulating protein. Science 266:117-119, 1994b
45. Wang MH, Skeel A, Leonard EJ: Proteolytic cleavage and activation of promacrophage-stimulating protein by resident peritoneal macrophage membrane proteases. J Clin Invest 97:720-727, 1996b
46. Wang MH, Yoshimura T, Skeel A, Leonard EJ: Proteolytic conversion of single chain precursor macrophage-stimulating protein to a biologically active heterodimer by contact enzymes of the coagulation cascade. J Biol Chem 269:3436-3440, 1994c
47. Yoshikawa W, Hara H, Takehara T, et al: Characterization of free alpha- and beta-chains of recombinant macrophage-stimulating protein. Arch Biochem Biophys 363:356-360, 1999
48. Yoshimura T, Yunki N, Wang MH, Skeel A, Leonard EJ: Cloning, sequencing, and expression of human macrophage stimulating protein (MSP, MST1) confirms MSP as a member of the family of kringle proteins and locates the MSP gene on chromosome 3. J Biol Chem 268:15461-15468, 1993