The Nf1 tumor suppressor regulates mouse skin wound healing, fibroblast proliferation, and collagen deposited by fibroblasts

Journal of Investigative Dermatology

Volumn 112, Issue 6, 1999, Pages 835-842

  Atit, Radhika P ^a   Crowe, Maria J ^b   Greenhalgh, David G ^c   Wenstrup, Richard J ^a   Ratner, Nancy ^a,b  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Epidermal growth factor; Macrophage; Neurofibromin; Ras

Indexed keywords

COLLAGEN; CYTOKINE; GENE PRODUCT; PROTEIN NF1; RAS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; FIBROBLAST; GENE MUTATION; MACROPHAGE; MALE; MOUSE; NEUROFIBROMATOSIS; NONHUMAN; PRIORITY JOURNAL; SKIN INJURY; TUMOR SUPPRESSOR GENE; WOUND HEALING;

EID: 0033001620     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1523-1747.1999.00609.x     Document Type: Article

References (56)

1. Basu TN, Gutmann DH, Fletcher JA, Glover TW, Collins FS, Downward J: Aberrant regulation of ras proteins in malignant tumour cells from type 1 neurofibromatosis patients. Nature 356:713-715, 1992
2. Berg RA: Determination of 3- and 4-hydroxyproline. Methods Enzymol 82:372-398, 1982
3. Brannan CI, Perkins AS, Vogel KS, et al: Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest derived tissues. Genes Dev 8:1019-1029, 1994
4. Brown RL, Breeden MP, Greenhalgh DG: PDW and TGFalpha act synergistically to improve wound healing in genetically diabetic mouse. J Surg Res 56:562-570, 1994
5. Clark RA. Mechanisms of cutaneous wound repair. In: Fitzpatrick TB, Eisen AZ, Wolff K, Freedberg IM, Austen KF (eds). Dermatology in General Medicine. New York: McGraw-Hill, 1993, pp 473-486
6. Colman SD, Williams CA, Wallace MR: Benign neurofibromas in type I neurofibromatosis (NF 1) show somatic deletions of the NF1 gene. Nature Genet 11:90-92, 1995
7. Daub H, Weiss FU, Wallasch C, Ullrich A: Role of transactivation of the EW receptor in signalling by G-protein-coupled receptors. Nature 379:557-560, 1996
8. DeClue JE, Papageorge AG, Fletcher JA, Dieffi SR, Ratner N, Vass WC, Lowy DR: Abnormal regulation of mammalian p2, 1 ras contributes to malignant tumor growth in von Recklinghausen (type 1) neurofibromatosis. Cell 69:265-273, 1992
9. Diegelman RF, Cohen IK, Kaplan AM: The role of macrophages in wound repair: a review. Plast Reconstr Surg 68:107-113, 1981
10. Dudley DT, Pang S, Decker J, Bridges AJ, Saltiel AR: A synthetic inhibitor of the mitogenactivated protein kinase cascade. Proc Natl Acad Sci, USA 92:7686-7689, 1995
11. Dunn NR, Winner GE, Hargett LY, Schrick JJ, Fogo AB, Hogan BLM: Haploinsufficient phenotypes in Bmp4 heterozygous null mice and modification by mutations in G13 and AIX4. Dev Biol 188:235-247, 1997
12. Dvorak HF: Tumors: wounds that do not heal. N Engl J Med 315:1650-1659, 1986
13. Easton DF, Ponder MA, Huson SM, Ponder BAJ: An analysis of variation in expression of neurofibromatosis type 1 (NFI): evidence for modifying genes. Am J Hum Genet 53:305-313, 1993
14. Eldridge CF, Bunge MB, Bunge RP, Wood PM: Differentiation of axon-related Schwann cells in view. Ascorbic acid regulates basal lamina assembly and myelin formation. J Cell Biol 105:1023-1034, 1987
15. Friedman JM, Birch PH: Type I neurofibromatosis: a descriptive analysis of the disorder in 1,728 patients. Am J Med Genet 70:138-143, 1997
16. Gailit J, Clark RA: Wound repair in the context of extracellular matrix. Curr Opin Cell Biol 6:717-725, 1994
17. Goldring MB, Goldring SR: Cytokines and growth control. Crit Rep Eukaryotic Gene Exp 1:301-326, 1991
18. Greenhalgh DG, Sprugel KH, Murray MJ, Ross R: PDGF and FGF stimulate wound healing in the genetically diabetic mouse. Am J Pathol 136:1235-1246, 1990
19. Griesser J, Kaufmann D, Maier B, Mailhammer R, Kuehl P, Krone W: Post-transcriptional regulation of neurofibromin level in cultured human melanocytes in response to growth factors. J Invest Dermatol 108:275-280, 1997
20. Griffin FM, Silverstein SC: Segmental response of the macrophage plasma membrane to a phagocytic stimulus. J Exp Med 139:323-327, 1974
21. Grotendorst GR: Chemoattractants and growth factors. In: Cohen IK, Diegelmann RF, Lindbald WJ (eds). Wound Healing: Biochemical and Clinical Aspects. Philadelphia, PA: Harcourt Brace Jovanovich, 1992, pp 237-246
22. Guha A, Lau N, Huvan I, Gutmann D, Provias J, Pawson T, Boss G: Ras-GTP levels are elevated in human NF1 peripheral nerve tumors. Oncogene 12:507-513, 1996
23. Guo HF, The I, Hannan F, Bernards A, Zliong Y: Requirement of Drosophila NF1 for activation of adenylyl cyclase by PACAP3, 8-like neuropeptides. Science 276:795-798, 1997
24. Hatamochi A, Ono M, Ueki H, Namba M: Regulation of collagen gene expression by transformed human fibroblasts: decreased type 1 and type III collagen RNA transcription. J Invest Dermatol 96:473-477, 1991
25. Hermonen J, Hirvonen O, Ylä Outinen H, et al: Neurofibromin: expression by normal human keratinocytes in vivo and in vitro and in epidermal malignancies. Lab Invest 73:221-228, 1995
26. Horan GS, Wu K, Wolgemuth D, Behringer RR: Homeotic transformation of cervical vertebrae in Hoxa-4 mutant mice. Proc Natl Acad Sci USA 91:12644-12648, 1994
27. Husmann L, Soulet L, Gautron J, Martelly I, Barritault D: Growth factors in skeletal muscle regeneration. Cytokine Growth Factor Rev 7:249-258, 1996
28. Huson SM, Clark P, Compston DAS, Harper PS: A genetic study of von Recklinghausen neurofibromatosis in south cast Wales I. Prevalence, mutation rate, and effect of parental transmission on severity. J Med Genet 26:704-711, 1989
29. Jaakkola S, Peltonen J, Riccardi V, Chu ML, Uitto J: Type I neurofibromatosis: selective expression of extracellular matrix genes by Schwann cells, perineurial cells, and fibroblasts in mixed cultures. J Clin Invest 84:253-261, 1989
30. Jacks T, Shih TS, Schmitt EM, Bronson RT, Bernards A, Weinberg RA: Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nature Genet 7:353-361, 1994
31. Johnson MR, Look AT, DeClue JE, Valentine MB, Lowy DR: Inactivation of the NF 1 gene in human melanoma and neuroblastoma cell lines without impaired regulation of GTPaRas. Proc Natl Acad Sci USA 90:5539-55433, 1993
32. Kenyon K, Contente S, Trackman PC, Tang J, Kagan HM, Friedman RM: Lysyl oxidase and rrg messenger RNA. Sci 253:802, 1991
33. Kim MR, Tamanoi F. Neurofibromatosis 1 GTPase activating protein-related domain and its functional significance. In: Upadhyaya M, Cooper D (eds). Neurofibromatosis Type I: from Genotype to Phenotype. Oxford: BIOS Scientific Publishers Ltd, 1998
34. Kim H, Rosenbaum T, Marchionni M, Ratner N, DeClue JE: Schwann cells from neurofibromin deficient mice exhibit activation of p21ras, inhibition of cell proliferation and morphological changes. Oncogene 11:325-335, 1995
35. Kim HA, Ling B, Ratner N: Nf1-deficient mouse Schwann cells are angiogenic and invasive and can be induced to hyperproliferate: reversion of some phenotypes by an inhibitor of famesyl protein transferase. Mol Cell Biol 17:862-872, 1997
36. Kobayashi M, Hashimoto N, Hoshino M, Hattori S, Iwashita S: Differential contribution of M(r) 120kDa rasGTPase-activating protein and neurofibromatosis type 1 gene product during the transition from growth phase to arrested state in human fibroblasts accompanied by a unique rasGTPase-activity. FEBS Lett 327:177-182, 1993
37. Konomi H, Arima M, Tanaka H, Hayashi T, Ikeda S: Increased deposition of types III and V collagens in neurofibroma tissue from patients with von Recklinghausen disease. Brain Dev 11:378-382, 1989
38. Largaespada DA, Brannan CI, Jenkins NA, Copeland NG: Nf1 deficiency causes Ras-mediated granulocyte/macrophage colony stimulating factor hypersensitivity and chronic myeloid leukemia. Nat Genet 12:137-143, 1996
39. Malhotra R, Ratner N: Localization of neurofibromin to keratinocytes and melanocytes in developing rat and human skin. J Invest Dermatol 102:812-818, 1994
40. Martin P: Wound healing-aiming for perfect skin regeneration. Science 276:75-81, 1997
41. Mast BA. The skin. In: Cohen IKRFD, Lindbald WJ (eds). Wound Healing Biochemical and Clinical Aspects. Philadelphia: Harcourt Brace Jovanovich, 1992, pp 344-355
42. Norris JFB, Fletcher AG, Marshall PJ, Hand MJ: Neurofibromatous dermal hyperplasia: a clinical, pharmacological, and ultrastructural study. Br J Dermatol 112:435-441, 1985
43. Peltonen J, Martala T, Vihersaari T, Renvall S, Pentinnen R: Collagen synthesis in cells cultured from v. Recklinghausen's neurofibromatosis. Acta Neuropathol (Berl) 55:183-187, 1981
44. Peltonen J, Penttinen R, Laijava H, Aho HJ. Collagens in neurofibromas and neurofibroma cell cultures. In: Rubenstein AE, Bunge RP, Housman DE (eds). Neurofibromatosis. Annals of the New York Academy of Sciences, Vol. 486. New York: New York Academy of Sciences, 1986, pp 260-270
45. Peltonen J, Jaakola S, Lebwohl M: Cellular differentiation and expression of matrix genes in type 1 neurofibromatosis. Lab Invest 59:760-771, 1988
46. Rappole DA, Mark D, Banda MJ, Werb Z: Wound macrophages express TGF-alpha and other growth factors in vivo: analysis by mRNA phenotyping. Science 241:708-711, 1988
47. Riccardi VM. Neurofibromatosis: Phenotype, Natural History and Pathogenesis. Baltimore: Johns Hopkins University Press, 1992
48. Rosenbaum T, Boissy YL, Kombrinck K, Brannan CI, Jenkins NA, Copeland NG, Ratner N: Neurofibromin-deficient fibroblasts fail to form perineurium in vitro. Development 121:3583-3592, 1995
49. Rosenbaum T, Patrie KM, Ratner N: Neurofibromatosis type 1: genetic and cellular mechanisms of peripheral nerve tumor formation. Neuroscientist 3:412-420, 1997
50. Sasaki T, Katsuhiko A, Nagai Y: Growth and collagen synthesis of cultured neurofibroma fibroblasts. J Dermatol 19:598-601, 1992
51. Sawada S, Florell S, Purandare SM, Ota M, Stephens K, Viskochil D: Identification of NF1 mutations; in both alleles of a dermal neurofibroma. Nature Genet 14:110-112, 1996
52. Slack JL, Parker MI, Robinson VR, Bornstein P: Regulation of collagen I gene expression by ras. Mol Cell Biol 12:4714-4723, 1992
53. Sollberg S, Muona P, Lebwohl M, Peltonen J, Uitto J: Presence of type I and VI collagen mRNAs in endothelial cells in cutaneous neurofibromas. Lab Invest 65:237-242, 1991
54. Uitto J, Matsuoka LY, Chu M, Pihlajaniemi T, Prockop D. Connective tissue biochemistry of neurofibromas. In: Rubenstein AE, Bunge RP, Housman DE (eds). Neurofibromatosis. Annals of the New York Academy of Sciences, Vol. 486. New York: New York Academy of Sciences, 1986. pp 271-286
55. Vogel KS, Brannan CI, Jerkins NA, Copeland NG, Parada LF: Loss of neurofibromin results in neurotrophin-independent survival of embryonic sensory and sympathetic neurons. Cell 82: 733-742., 1995
56. Ylä-Outinen HY, Aaltonen V, Björkstrand A, et al: Upregulation of tumor suppressor protein neurofibromin in normal wound healing and in vitro evidence for platelet derived growth factor (P13GF) and transforming growth factor-beta 1 (TGF-1) elicited increase in neurofibromin mRNA steady-state levels in dermal fibroblasts. J Invest Dermatol 110:232-237, 1998