Collagen/annexin V Interactions Regulate Chondrocyte Mineralization

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2008 Feb 19

PMID 18281278

Citations 18

Authors

Hyon Jong Kim

Thorsten Kirsch

Affiliations

Soon will be listed here.

Abstract

Physiological mineralization in growth plate cartilage is highly regulated and restricted to terminally differentiated chondrocytes. Because mineralization occurs in the extracellular matrix, we asked whether major extracellular matrix components (collagens) of growth plate cartilage are directly involved in regulating the mineralization process. Our findings show that types II and X collagen interacted with cell surface-expressed annexin V. These interactions led to a stimulation of annexin V-mediated Ca(2+) influx resulting in an increased intracellular Ca(2+) concentration, [Ca(2+)](i), and ultimately increased alkaline phosphatase activity and mineralization of growth plate chondrocytes. Consequently, stimulation of these interactions (ascorbate to stimulate collagen synthesis, culturing cells on type II collagen-coated dishes, or overexpression of full-length annexin V) resulted in increase of [Ca(2+)](i), alkaline phosphatase activity, and mineralization of growth plate chondrocytes, whereas inhibition of these interactions (3,4-dehydro-l-proline to inhibit collagen secretion, K-201, a specific annexin channel blocker, overexpression of N terminus-deleted mutant annexin V that does not bind to type II collagen and shows reduced Ca(2+) channel activities) decreased [Ca(2+)](i), alkaline phosphatase activity, and mineralization. In conclusion, the interactions between collagen and annexin V regulate mineralization of growth plate cartilage. Because annexin V is up-regulated during pathological mineralization events of articular cartilage, it is possible that these interactions also regulate pathological mineralization.

Citing Articles

Annexin A5 derived from matrix vesicles protects against osteoporotic bone loss via mineralization.

Su G, Zhang D, Li T, Pei T, Yang J, Tu S Bone Res. 2023; 11(1):60.

PMID: 37940665 PMC: 10632518. DOI: 10.1038/s41413-023-00290-9.

Annexin A5 stabilizes matrix vesicle-biomimetic lipid membranes: unravelling a new role of annexins in calcification.

Ferreira C, Cruz M, Bolean M, Andrilli L, Millan J, Ramos A Eur Biophys J. 2023; 52(8):721-733.

PMID: 37938350 PMC: 10682239. DOI: 10.1007/s00249-023-01687-4.

Calcium-Dependent Cytosolic Phospholipase A2α as Key Factor in Calcification of Subdermally Implanted Aortic Valve Leaflets.

Bonetti A, Contin M, Tonon F, Marchini M, Ortolani F Int J Mol Sci. 2022; 23(4).

PMID: 35216105 PMC: 8877272. DOI: 10.3390/ijms23041988.

Augmentation of and Suppression of Expression in the Pituitary Gland of Female Annexin A5 Null Mouse.

Terashima R, Saigo T, Laoharatchatathanin T, Kurusu S, Brachvogel B, Poschl E J Endocr Soc. 2020; 4(9):bvaa096.

PMID: 32864544 PMC: 7448937. DOI: 10.1210/jendso/bvaa096.

Matrix vesicle biomimetics harboring Annexin A5 and alkaline phosphatase bind to the native collagen matrix produced by mineralizing vascular smooth muscle cells.

Bolean M, Izzi B, van Kerckhoven S, Bottini M, Ramos A, Millan J Biochim Biophys Acta Gen Subj. 2020; 1864(8):129629.

PMID: 32360152 PMC: 8370721. DOI: 10.1016/j.bbagen.2020.129629.

References

Siever D, Erickson H . Extracellular annexin II. Int J Biochem Cell Biol. 1998; 29(11):1219-23. DOI: 10.1016/s1357-2725(97)00057-5. View

Aigner T, Bertling W, Stoss H, Weseloh G, von der Mark K . Independent expression of fibril-forming collagens I, II, and III in chondrocytes of human osteoarthritic cartilage. J Clin Invest. 1993; 91(3):829-37. PMC: 288034. DOI: 10.1172/JCI116303. View

Abe T, Abe Y, Aida Y, Hara Y, Maeda K . Extracellular matrix regulates induction of alkaline phosphatase expression by ascorbic acid in human fibroblasts. J Cell Physiol. 2001; 189(2):144-51. DOI: 10.1002/jcp.10011. View

Chung C, Erickson H . Cell surface annexin II is a high affinity receptor for the alternatively spliced segment of tenascin-C. J Cell Biol. 1994; 126(2):539-48. PMC: 2200039. DOI: 10.1083/jcb.126.2.539. View

Takagi H, Asano Y, Yamakawa N, Matsumoto I, Kimata K . Annexin 6 is a putative cell surface receptor for chondroitin sulfate chains. J Cell Sci. 2002; 115(Pt 16):3309-18. DOI: 10.1242/jcs.115.16.3309. View

Aurich M, Robin Poole A, Reiner A, Mollenhauer C, Margulis A, Kuettner K . Matrix homeostasis in aging normal human ankle cartilage. Arthritis Rheum. 2002; 46(11):2903-10. DOI: 10.1002/art.10611. View

Grynkiewicz G, Poenie M, Tsien R . A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985; 260(6):3440-50. View

Harada S, Matsumoto T, Ogata E . Role of ascorbic acid in the regulation of proliferation in osteoblast-like MC3T3-E1 cells. J Bone Miner Res. 1991; 6(9):903-8. DOI: 10.1002/jbmr.5650060902. View

Mollenhauer J, Bee J, Lizarbe M, von der Mark K . Role of anchorin CII, a 31,000-mol-wt membrane protein, in the interaction of chondrocytes with type II collagen. J Cell Biol. 1984; 98(4):1572-9. PMC: 2113202. DOI: 10.1083/jcb.98.4.1572. View

10.

Kaneko N, Ago H, Matsuda R, Inagaki E, Miyano M . Crystal structure of annexin V with its ligand K-201 as a calcium channel activity inhibitor. J Mol Biol. 1998; 274(1):16-20. DOI: 10.1006/jmbi.1997.1375. View

11.

Berendes R, Burger A, Voges D, Demange P, Huber R . Calcium influx through annexin V ion channels into large unilamellar vesicles measured with fura-2. FEBS Lett. 1993; 317(1-2):131-4. DOI: 10.1016/0014-5793(93)81507-v. View

12.

Kivirikko K, Myllyla R . Recent developments in posttranslational modification: intracellular processing. Methods Enzymol. 1987; 144:96-114. DOI: 10.1016/0076-6879(87)44175-x. View

13.

REID D, AYDELOTTE M, Mollenhauer J . Cell attachment, collagen binding, and receptor analysis on bovine articular chondrocytes. J Orthop Res. 2000; 18(3):364-73. DOI: 10.1002/jor.1100180307. View

14.

Zuscik M, DSouza M, Ionescu A, Gunter K, Gunter T, OKeefe R . Growth plate chondrocyte maturation is regulated by basal intracellular calcium. Exp Cell Res. 2002; 276(2):310-9. DOI: 10.1006/excr.2002.5527. View

15.

Mollenhauer J, Mok M, King K, Gupta M, Chubinskaya S, Koepp H . Expression of anchorin CII (cartilage annexin V) in human young, normal adult, and osteoarthritic cartilage. J Histochem Cytochem. 1999; 47(2):209-20. DOI: 10.1177/002215549904700209. View

16.

Mills D, Daniel J . Development of functional specializations within the maturing rabbit flexor digitorum profundus tendon. Connect Tissue Res. 1993; 30(1):37-57. DOI: 10.3109/03008209309032929. View

17.

Iannotti J, Brighton C . Cytosolic ionized calcium concentration in isolated chondrocytes from each zone of the growth plate. J Orthop Res. 1989; 7(4):511-8. DOI: 10.1002/jor.1100070408. View

18.

Meier S, Solursh M . Ultrastructural analysis of the effect of ascorbic acid on secretion and assembly of extracellular matrix by cultured chick embryo chondrocytes. J Ultrastruct Res. 1978; 65(1):48-59. DOI: 10.1016/s0022-5320(78)90021-7. View

19.

Wang W, Xu J, Kirsch T . Annexin-mediated Ca2+ influx regulates growth plate chondrocyte maturation and apoptosis. J Biol Chem. 2002; 278(6):3762-9. DOI: 10.1074/jbc.M208868200. View

20.

Kirsch T, Swoboda B, Nah H . Activation of annexin II and V expression, terminal differentiation, mineralization and apoptosis in human osteoarthritic cartilage. Osteoarthritis Cartilage. 2000; 8(4):294-302. DOI: 10.1053/joca.1999.0304. View