Sex-Linked Skeletal Phenotype of Lysyl Oxidase Like-1 Mutant Mice

Calcified Tissue International

Volumn 98, Issue 2, 2016, Pages 172-185

  Alsofi, Loai ^a,b   Daley, Eileen ^a   Hornstra, Ian ^c   Morgan, Elise F ^d   Mason, Zachary D ^d   Acevedo, Jesus F ^e   Word, R Ann ^e   Gerstenfeld, Louis C ^f   Trackman, Philip C ^a  

^a BOSTON UNIVERSITY   (United States)

^b KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Boston University   (United States)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^f BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bone histomorphometry; Collagen; Genetic animal model; Lysyl oxidases; Micro comuted tomography

Indexed keywords

COLLAGEN; INTERLEUKIN 6; LYSSY LOXIDASE LIKE 1; OSTEOCALCIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PROTEIN LYSINE 6 OXIDASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; LOXL1 PROTEIN, MOUSE; OXIDOREDUCTASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE STRUCTURE; BONE TURNOVER; CARTILAGE CELL; CODON; FEMALE; FEMUR METAPHYSIS; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PHENOTYPE; PRIORITY JOURNAL; TIBIA; TRABECULAR BONE; WILD TYPE; ANIMAL; BONE; BONE DENSITY; C57BL MOUSE; COMPUTER ASSISTED DIAGNOSIS; DEFICIENCY; DIAGNOSTIC IMAGING; IMMUNOASSAY; KNOCKOUT MOUSE; METABOLISM; MICRO-COMPUTED TOMOGRAPHY; PHYSIOLOGY; SEXUAL DEVELOPMENT; SITE DIRECTED MUTAGENESIS;

AMINO ACID OXIDOREDUCTASES; ANIMALS; BONE AND BONES; BONE DENSITY; FEMALE; IMMUNOASSAY; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTAGENESIS, SITE-DIRECTED; PHENOTYPE; RADIOGRAPHIC IMAGE INTERPRETATION, COMPUTER-ASSISTED; SEX CHARACTERISTICS; X-RAY MICROTOMOGRAPHY;

EID: 84955749742     PISSN: 0171967X     EISSN: 14320827     Source Type: Journal    
DOI: 10.1007/s00223-015-0076-4     Document Type: Article

References (56)

1. Csiszar K (2001) Lysyl oxidases: a novel multifunctional amine oxidase family. Prog Nucleic Acid Res Mol Biol 70:1–32
2. Khosravi R, Sodek KL, Xu WP, Bais MV, Saxena D, Faibish M, Trackman PC (2014) A novel function for lysyl oxidase in pluripotent mesenchymal cell proliferation and relevance to inflammation-associated osteopenia. PLoS One 9:e100669
3. Perryman L, Erler JT (2014) Lysyl oxidase in cancer research. Future Oncol 10:1709–1717
4. Kenyon K, Contente S, Trackman PC, Tang J, Kagan HM, Friedman RM (1991) Lysyl oxidase and rrg messenger RNA. Science 253:802
5. Liu G, Daneshgari F, Li M, Lin D, Lee U, Li T, Damaser MS (2007) Bladder and urethral function in pelvic organ prolapsed lysyl oxidase like-1 knockout mice. Br J Urol Int 100:414–418
6. Panchenko MV, Stetler-Stevenson WG, Trubetskoy OV, Gacheru SN, Kagan HM (1996) Metalloproteinase activity secreted by fibrogenic cells in the processing of prolysyl oxidase. Potential role of procollagen C-proteinase. J Biol Chem 271:7113–7119
7. Trackman PC, Bedell-Hogan D, Tang J, Kagan HM (1992) Post-translational glycosylation and proteolytic processing of a lysyl oxidase precursor. J Biol Chem 267:8666–8671
8. Uzel MI, Scott IC, Babakhanlou-Chase H, Palamakumbura AH, Pappano WN, Hong HH, Greenspan DS, Trackman PC (2001) Multiple bone morphogenetic protein 1-related mammalian metalloproteinases process pro-lysyl oxidase at the correct physiological site and control lysyl oxidase activation in mouse embryo fibroblast cultures. J Biol Chem 276:22537–22543
9. Liu X, Zhao Y, Gao J, Pawlyk B, Starcher B, Spencer JA, Yanagisawa H, Zuo J, Li T (2004) Elastic fiber homeostasis requires lysyl oxidase-like 1 protein. Nat Genet 36:178–182
10. Wieslander CK, Rahn DD, McIntire DD, Acevedo JF, Drewes PG, Yanagisawa H, Word RA (2009) Quantification of pelvic organ prolapse in mice: vaginal protease activity precedes increased MOPQ scores in fibulin 5 knockout mice. Biol Reprod 80:407–414
11. Kagan HM, Trackman PC (1991) Properties and function of lysyl oxidase. Am J Respir Cell Mol Biol 5:206–210
12. Smith-Mungo LI, Kagan HM (1998) Lysyl oxidase: properties, regulation and multiple functions in biology. Matrix Biol J Int Soc Matrix Biol 16:387–398
13. Siegel RC (1979) Lysyl oxidase. Int Rev Connect Tissue Res 8:73–118
14. Kagan HM (1986) Characterization and regulation of lysyl oxidase. In: Mecham RP (ed) Regulation of matrix accumulation. Academic Press, San Diego, pp 321–398
15. Hornstra IK, Birge S, Starcher B, Bailey AJ, Mecham RP, Shapiro SD (2003) Lysyl oxidase is required for vascular and diaphragmatic development in mice. J Biol Chem 278:14387–14393
16. Maki JM, Rasanen J, Tikkanen H, Sormunen R, Makikallio K, Kivirikko KI, Soininen R (2002) Inactivation of the lysyl oxidase gene Lox leads to aortic aneurysms, cardiovascular dysfunction, and perinatal death in mice. Circulation 106:2503–2509
17. Pischon N, Maki JM, Weisshaupt P, Heng N, Palamakumbura AH, N’Guessan P, Ding A, Radlanski R, Renz H, Bronckers TA, Myllyharju J, Kielbassa AM, Kleber BM, Bernimoulin JP, Trackman PC (2009) Lysyl oxidase (lox) gene deficiency affects osteoblastic phenotype. Calcif Tissue Int 85:119–126
18. Simon LS (2007) Osteoporosis. Rheum Dis Clin N Am 33:149–176
19. Shih MS, Cook MA, Spence CA, Palnitkar S, McElroy H, Parfitt AM (1993) Relationship between bone formation rate and osteoblast surface on different subdivisions of the endosteal envelope in aging & osteoporosis. Bone 14:519–521
20. Sanada H, Shikata J, Hamamoto H, Ueba Y, Yamamuro T, Takeda T (1978) Changes in collagen cross-linking and lysyl oxidase by estrogen. Biochim Biophys Acta 541:408–413
21. Saito M, Marumo K (2010) Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int 21:195–214
22. Atsawasuwan P, Mochida Y, Parisuthiman D, Yamauchi M (2005) Expression of lysyl oxidase isoforms in MC3T3-E1 osteoblastic cells. Biochem Biophys Res Commun 327:1042–1046
23. Assaggaf MA, Kantarci A, Sume SS, Trackman PC (2015) Prevention of phenytoin-induced gingival overgrowth by lovastatin in mice. Am J Pathol 185:1588–1599
24. Morgan EF, Mason ZD, Chien KB, Pfeiffer AJ, Barnes GL, Einhorn TA, Gerstenfeld LC (2009) Micro-computed tomography assessment of fracture healing: relationships among callus structure, composition, and mechanical function. Bone 44:335–344
25. Gere JM, Goodno BJ (2009) Mechanics of materials. Cengage Learning Inc., Independence
26. Buie HR, Campbell GM, Klinck RJ, MacNeil JA, Boyd SK (2007) Automatic segmentation of cortical and trabecular compartments based on a dual threshold technique for in vivo micro-CT bone analysis. Bone 41:505–515
27. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Muller R (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 25:1468–1486
28. Junqueira LC, Bignolas G, Brentani RR (1979) Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 11:447–455
29. Vasikaran S, Eastell R, Bruyere O, Foldes AJ, Garnero P, Griesmacher A, McClung M, Morris HA, Silverman S, Trenti T, Wahl DA, Cooper C, Kanis JA (2011) Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int 22:391–420
30. Iftikhar M, Hurtado P, Bais MV, Wigner N, Stephens DN, Gerstenfeld LC, Trackman PC (2011) Lysyl oxidase-like-2 (LOXL2) is a major isoform in chondrocytes and is critically required for differentiation. J Biol Chem 286:909–918
31. Martin A, Salvador F, Moreno-Bueno G, Floristan A, Ruiz-Herguido C, Cuevas EP, Morales S, Santos V, Csiszar K, Dubus P, Haigh JJ, Bigas A, Portillo F, Cano A (2015) Lysyl oxidase-like 2 represses Notch1 expression in the skin to promote squamous cell carcinoma progression. EMBO J 34:1090–1109
32. Tommasini SM, Morgan TG, van der Meulen M, Jepsen KJ (2005) Genetic variation in structure-function relationships for the inbred mouse lumbar vertebral body. J Bone Miner Res 20:817–827
33. Lee UJ, Gustilo-Ashby AM, Daneshgari F, Kuang M, Vurbic D, Lin DL, Flask CA, Li T, Damaser MS (2008) Lower urogenital tract anatomical and functional phenotype in lysyl oxidase like-1 knockout mice resembles female pelvic floor dysfunction in humans. Am J Physiol Renal Physiol 295:F545–F555
34. Kapczuk K, Sowinska-Przepiera E, Friebe Z (2003) Osteoprotegerin/RANKL/RANK system and postmenopausal osteoporosis. The possible therapeutic aspects. Ginekol Pol 74:323–331
35. Bouxsein ML, Myers KS, Shultz KL, Donahue LR, Rosen CJ, Beamer WG (2005) Ovariectomy-induced bone loss varies among inbred strains of mice. J Bone Mine Res 20:1085–1092
36. Bord S, Ireland DC, Beavan SR, Compston JE (2003) The effects of estrogen on osteoprotegerin, RANKL, and estrogen receptor expression in human osteoblasts. Bone 32:136–141
37. Boyce BF, Xing L (2007) Biology of RANK, RANKL, and osteoprotegerin. Arthritis Res Ther 9(Suppl 1):S1
38. Bronson RE, Calaman SD, Traish AM, Kagan HM (1987) Stimulation of lysyl oxidase (EC 1.4.3.13) activity by testosterone and characterization of androgen receptors in cultured calf aorta smooth-muscle cells. Biochem J 244:317–323
39. Ballanti P, Minisola S, Pacitti MT, Scarnecchia L, Rosso R, Mazzuoli GF, Bonucci E (1997) Tartrate-resistant acid phosphate activity as osteoclastic marker: sensitivity of cytochemical assessment and serum assay in comparison with standardized osteoclast histomorphometry. Osteoporos Int 7:39–43
40. Biver E (2012) Use of bone turnover markers in clinical practice. Curr Opin Endocrinol Diabetes Obes 19:468–473
41. Garnero P, Ferreras M, Karsdal MA, Nicamhlaoibh R, Risteli J, Borel O, Qvist P, Delmas PD, Foged NT, Delaissé JM (2003) The type I collagen fragments ICTP and CTX reveal distinct enzymatic pathways of bone collagen degradation. J Bone Miner Res 18:859–867
42. Koivula M-K, Risteli L, Risteli J (2012) Measurement of aminoterminal propeptide of type I procollagen (PINP) in serum. Clin Biochem 45:920–927
43. Christiansen DL, Huang EK, Silver FH (2000) Assembly of type I collagen: fusion of fibril subunits and the influence of fibril diameter on mechanical properties. Matrix Biol 19:409–420
44. Muiznieks LD, Keeley FW (2013) Molecular assembly and mechanical properties of the extracellular matrix: a fibrous protein perspective. Biochim Biophys Acta 1832:866–875
45. Ottani V, Raspanti M, Ruggeri A (2001) Collagen structure and functional implications. Micron 32:251–260
46. Gualeni B, Rajpar MH, Kellogg A, Bell PA, Arvan P, Boot-Handford RP, Briggs MD (2013) A novel transgenic mouse model of growth plate dysplasia reveals that decreased chondrocyte proliferation due to chronic ER stress is a key factor in reduced bone growth. Dis Models Mech 6:1414–1425
47. Wang G, Woods A, Agoston H, Ulici V, Glogauer M, Beier F (2007) Genetic ablation of Rac1 in cartilage results in chondrodysplasia. Dev Biol 306:612–623
48. Lucero HA, Ravid K, Grimsby JL, Rich CB, DiCamillo SJ, Maki JM, Myllyharju J, Kagan HM (2008) Lysyl oxidase oxidizes cell membrane proteins and enhances the chemotactic response of vascular smooth muscle cells. J Biol Chem 283:24103–24117
49. Atsawasuwan P, Mochida Y, Katafuchi M, Kaku M, Fong KS, Csiszar K, Yamauchi M (2008) Lysyl oxidase binds transforming growth factor-beta and regulates its signaling via amine oxidase activity. J Biol Chem 283:34229–34240
50. Li W, Nugent MA, Zhao Y, Chau AN, Li SJ, Chou IN, Liu G, Kagan HM (2003) Lysyl oxidase oxidizes basic fibroblast growth factor and inactivates its mitogenic potential. J Cell Biochem 88:152–164
51. Le Provost GS, Debret R, Cenizo V, Aimond G, Pez F, Kaniewski B, Andre V, Sommer P (2010) Lysyl oxidase silencing impairs keratinocyte differentiation in a reconstructed-epidermis model. Exp Dermatol 19:1080–1087
52. Palamakumbura AH, Vora SR, Nugent MA, Kirsch KH, Sonenshein GE, Trackman PC (2009) Lysyl oxidase propeptide inhibits prostate cancer cell growth by mechanisms that target FGF-2-cell binding and signaling. Oncogene 28:3390–3400
53. Kirschmann DA, Seftor EA, Fong SF, Nieva DR, Sullivan CM, Edwards EM, Sommer P, Csiszar K, Hendrix MJ (2002) A molecular role for lysyl oxidase in breast cancer invasion. Cancer Res 62:4478–4483
54. Li J, Gu X, Ma Y, Calicchio ML, Kong D, Teng YD, Yu L, Crain AM, Vartanian TK, Pasqualini R, Arap W, Libermann TA, Snyder EY, Sidman RL (2010) Nna1 mediates Purkinje cell dendritic development via lysyl oxidase propeptide and NF-kappaB signaling. Neuron 68:45–60
55. Vora SR, Palamakumbura AH, Mitsi M, Guo Y, Pischon N, Nugent MA, Trackman PC (2010) Lysyl oxidase propeptide inhibits FGF-2-induced signaling and proliferation of osteoblasts. J Biol Chem 285:7384–7393
56. Uveges TE, Collin-Osdoby P, Cabral WA, Ledgard F, Goldberg L, Bergwitz C, Forlino A, Osdoby P, Gronowicz GA, Marini JC (2008) Cellular mechanism of decreased bone in Brtl mouse model of OI: imbalance of decreased osteoblast function and increased osteoclasts and their precursors. J Bone Miner Res 23:1983–1994