View Item 

Show simple item record

Proteoglycan 4: A dynamic regulator of skeletogenesis and parathyroid hormone skeletal anabolism
dc.contributor.authorNovince, Chad M.en_US
dc.contributor.authorMichalski, Megan Nen_US
dc.contributor.authorKoh, Amy J.en_US
dc.contributor.authorSinder, Benjamin Pen_US
dc.contributor.authorEntezami, Payamen_US
dc.contributor.authorEber, Matthew Ren_US
dc.contributor.authorPettway, Glenda Jen_US
dc.contributor.authorRosol, Thomas J.en_US
dc.contributor.authorWronski, Thomas Jen_US
dc.contributor.authorKozloff, Ken Men_US
dc.contributor.authorMcCauley, Laurie K.en_US
dc.date.accessioned2012-01-05T22:04:44Z
dc.date.available2013-03-04T15:29:53Zen_US
dc.date.issued2012-01en_US
dc.identifier.citationNovince, Chad M; Michalski, Megan N; Koh, Amy J; Sinder, Benjamin P; Entezami, Payam; Eber, Matthew R; Pettway, Glenda J; Rosol, Thomas J; Wronski, Thomas J; Kozloff, Ken M; McCauley, Laurie K (2012). "Proteoglycan 4: A dynamic regulator of skeletogenesis and parathyroid hormone skeletal anabolism." Journal of Bone and Mineral Research 27(1): 11-25. <http://hdl.handle.net/2027.42/89450>en_US
dc.identifier.issn0884-0431en_US
dc.identifier.issn1523-4681en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/89450
dc.description.abstractProteoglycan 4 ( Prg4 ), known for its lubricating and protective actions in joints, is a strong candidate regulator of skeletal homeostasis and parathyroid hormone (PTH) anabolism. Prg4 is a PTH‐responsive gene in bone and liver. Prg4 null mutant mice were used to investigate the impact of proteoglycan 4 on skeletal development, remodeling, and PTH anabolic actions. Young Prg4 mutant and wild‐type mice were administered intermittent PTH(1–34) or vehicle daily from 4 to 21 days. Young Prg4 mutant mice had decreased growth plate hypertrophic zones, trabecular bone, and serum bone formation markers versus wild‐type mice, but responded with a similar anabolic response to PTH. Adult Prg4 mutant and wild‐type mice were administered intermittent PTH(1–34) or vehicle daily from 16 to 22 weeks. Adult Prg4 mutant mice had decreased trabecular and cortical bone, and blunted PTH‐mediated increases in bone mass. Joint range of motion and animal mobility were lower in adult Prg4 mutant versus wild‐type mice. Adult Prg4 mutant mice had decreased marrow and liver fibroblast growth factor 2 (FGF‐2) mRNA and reduced serum FGF‐2, which were normalized by PTH. A single dose of PTH decreased the PTH/PTHrP receptor (PPR), and increased Prg4 and FGF‐2 to a similar extent in liver and bone. Proteoglycan 4 supports endochondral bone formation and the attainment of peak trabecular bone mass, and appears to support skeletal homeostasis indirectly by protecting joint function. Bone‐ and liver‐derived FGF‐2 likely regulate proteoglycan 4 actions supporting trabeculae formation. Blunted PTH anabolic responses in adult Prg4 mutant mice are associated with altered biomechanical impact secondary to joint failure. © 2012 American Society for Bone and Mineral Researchen_US
dc.publisherWiley Subscription Services, Inc., A Wiley Companyen_US
dc.subject.otherPTHen_US
dc.subject.otherPrg4en_US
dc.subject.otherBoneen_US
dc.subject.otherLiveren_US
dc.subject.otherFGF‐2en_US
dc.titleProteoglycan 4: A dynamic regulator of skeletogenesis and parathyroid hormone skeletal anabolismen_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelInternal Medicine and Specialitiesen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Periodontics and Oral Medicine, School of Dentistry, University of Michigan, Ann Arbor, MI, USAen_US
dc.contributor.affiliationumDepartment of Orthopaedic Surgery, Medical School, University of Michigan, Ann Arbor, MI, USAen_US
dc.contributor.affiliationumDepartment of Pathology, Medical School, University of Michigan, Ann Arbor, MI, USAen_US
dc.contributor.affiliationumProfessor and Chair, Department of Periodontics and Oral Medicine, the University of Michigan School of Dentistry, 1011 N. University Avenue, Ann Arbor, MI 48109.en_US
dc.contributor.affiliationotherDepartment of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, OH, USAen_US
dc.contributor.affiliationotherDepartment of Physiological Sciences, University of Florida, Gainesville, FL, USAen_US
dc.identifier.pmid21932346en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/89450/1/508_ftp.pdf
dc.identifier.doi10.1002/jbmr.508en_US
dc.identifier.sourceJournal of Bone and Mineral Researchen_US
dc.identifier.citedreferenceKousteni S, Bilezikian JP. Cellular actions of parathyroid hormone. In: Bilezikian JP, Raisz LG, Martin TJ, editors. Principles of bone biology. 3rd ed. Burlington, MA: Elsevier Press; 2008. p. 639 – 56.en_US
dc.identifier.citedreferenceAspenberg P, Genant HK, Johansson T, Nino AJ, See K, Krohn K, Garcia‐Hernandez PA, Recknor CP, Einhorn TA, Dalsky GP, Mitlak BH, Fierlinger A, Lakshmanan MC. Teriparatide for acceleration of fracture repair in humans: a prospective, randomized, double‐blind study of 102 postmenopausal women with distal radial fractures. J Bone Miner Res. 2010; 25: 404 – 14.en_US
dc.identifier.citedreferenceBashutski JD, Eber RM, Kinney JS, Benavides E, Maitra S, Braun TM, Giannobile WV, McCauley LK. Teriparatide and osseous regeneration in the oral cavity. N Eng J Med. 2010; 363: 2396 – 405.en_US
dc.identifier.citedreferenceHurley MM, Tetradis S, Huang YF, Hock J, Kream BE, Raisz LG. Parathyroid hormone regulates the expression of fibroblast growth factor‐2 mRNA and fibroblast growth factor receptor mRNA in osteoblastic cells. J Bone Miner Res. 1999; 14: 776 – 83.en_US
dc.identifier.citedreferenceWatson P, Lazowski D, Han V, Fraher L, Steer B, Hodsman A. Parathyroid hormone restores bone mass and enhances osteoblast insulin‐like growth factor 1 gene expression in ovariectomized rats. Bone. 1995; 16: 357 – 65.en_US
dc.identifier.citedreferenceBikle DD, Sakata T, Leary C, Elalieh H, Ginzinger D, Rosen CJ, Beamer WG, Majumdar S, Halloran BP. Insulin‐like growth factor I is required for the anabolic actions of parathyroid hormone on mouse bone. J Bone Miner Res. 2002; 17: 1570 – 8.en_US
dc.identifier.citedreferenceMiyakoshi N, Kasukawa Y, Linkhart TA, Baylink DJ, Mohan S. Evidence that anabolic effects of PTH on bone require IGF‐1 in growing mice. Endocrinology. 2001; 142: 4349 – 56.en_US
dc.identifier.citedreferenceHurley MM, Okada Y, Xiao L, Tanaka Y, Ito M, Okimoto N, Nakamura T, Rosen CJ, Doetschman T, Coffin JD. Impaired bone anabolic response to parathyroid hormone in Fgf2−/− and Fgf2+/− mice. Biochem Biophys Res Commun. 2006; 341: 989 – 94.en_US
dc.identifier.citedreferenceNovince CM, Koh AJ, Marchesan JT, McCauley LK. Proteoglycan‐4: a novel gene regulating parathyroid hormone actions in bone anabolism and hematopoiesis. ASBMR Annual Meeting, 2009, Denver, Colorado, USA. Abstract #1186. J Bone Miner Res. 2009; 24 (Suppl 1): Available at http://www.asbmr.org/Meetings/AnnualMeeting/AbstractDetail.aspx?aid=51d4e88b‐f79d‐47e2‐a15b‐134f0c57b52e. Accessed September 20, 2011.en_US
dc.identifier.citedreferenceNovince CM, Koh AJ, Michalski MN, Marchesan JT, Wang J, Jung Y, Berry JE, Eber MR, Rosol TJ, Taichman RS, McCauley LK. Proteoglycan‐4, a novel immunomodulatory factor, regulates parathyroid hormone actions on hematopoietic cells. Am J Pathol. 2011; Epub ahead of print. PMID: 21939632.en_US
dc.identifier.citedreferenceIkegawa S, Sano M, Koshizuka Y, Nakamura Y. Isolation, characterization and mapping of the mouse and human PRG4 (proteoglycan 4) genes. Cytogenet Genome Res. 2000; 90: 291 – 7.en_US
dc.identifier.citedreferenceRhee DK, Marcelino J, Baker M, Gong Y, Smits P, Lefebvre V, Jay GD, Stewart M, Wang H, Warman ML, Carpten JD. The secreted glycoprotein lubricin protects cartilage surfaces and inhibits synovial cell overgrowth. J Clin Invest. 2005; 115: 622 – 31.en_US
dc.identifier.citedreferenceLiu YJ, Lu SH, Xu B, Yang RC, Ren Q, Liu B, Li B, Lu M, Yan FY, Han ZB, Han ZC. Hemangiopoietin, a novel human growth factor for the primitive cells of both hematopoietic and endothelial cell lineages. Blood. 2004; 103: 4449 – 56.en_US
dc.identifier.citedreferenceMarcelino J, Carpten JD, Suwairi WM, Gutierrez OM, Schwartz S, Robbins C, Sood R, Makalowska I, Baxevanis A, Johnstone B, Laxer RM, Zemel L, Kim CA, Herd JK, Ihle J, Williams C, Johnson M, Raman V, Alonso LG, Brunoni D, Gerstein A, Papadopoulos N, Bahabri SA, Trent JM, Warman ML. CACP, encoding a secreted proteoglycan, is mutated in camptodactyly‐arthropathy‐coxa vara‐pericarditis syndrome. Nat Genet. 1999; 23: 319 – 22.en_US
dc.identifier.citedreferenceSchmittgen TD, Livak KJ. Analyzing real‐time PCR data by the comparative CT method. Nat Protoc. 2008; 3: 1101 – 8.en_US
dc.identifier.citedreferenceYakar S, Rosen CJ, Beamer WG, Ackert‐Bicknell CL, Wu Y, Liu JL, Ooi GT, Setser J, Frystyk J, Boisclair YR, Leroith D. Circulating levels of IGF‐1 directly regulate bone growth and density. J Clin Invest. 2002; 110: 771 – 81.en_US
dc.identifier.citedreferenceParfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. Bone histomorphometry: standardization of nomenclature, symbols and units (Report of the ASBMR Histomorphometry Nomenclature Committee). J Bone Miner Res. 1987; 2: 595 – 610.en_US
dc.identifier.citedreferenceBouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Muller R. Guidelines for assessment of bone microstructure in rodents using micro‐computed tomography. J Bone Miner Res. 2010; 25: 1468 – 86.en_US
dc.identifier.citedreferenceKoh AJ, Beecher CA, Rosol TJ, McCauley LK. Cyclic AMP activation in osteoblastic cells: effects on PTH‐1 receptors and osteoblastic differentiation in vitro. Endocrinology. 1999; 140: 3154 – 62.en_US
dc.identifier.citedreferenceTian J, Smogorezewski M, Kedes L, Massry SG. Parathyroid hormone‐parathyroid hormone related protein receptor messenger RNA is present in many tissues besides the kidney. Am J Nephrol. 1993; 13: 210 – 3.en_US
dc.identifier.citedreferenceWatson PH, Fraher LJ, Hendy GN, Chung UI, Kisiel M, Natale BV, Hodsman AB. Nuclear localization of the type 1 PTH/PTHrP receptor in rat tissues. J Bone Miner Res. 2000; 15: 1033 – 44.en_US
dc.identifier.citedreferenceSjögren K, Sheng M, Moverare S, Liu JL, Wallenius K, Tornell J, Isaksson O, Jansson JO, Mohan S, Ohlsson C. Effects of liver‐derived insulin‐like growth factor I on bone metabolism in mice. J Bone Miner Res. 2002; 17: 1977 – 87.en_US
dc.identifier.citedreferenceElis S, Courtland HW, Wu Y, Rosen CJ, Sun H, Jepsen KJ, Majeska RJ, Yakar S. Elevated serum levels of IGF‐1 are sufficient to establish normal body size and skeletal properties even in the absence of tissue IGF‐1. J Bone Miner Res. 2010; 25: 1257 – 66.en_US
dc.identifier.citedreferenceYakar S, Bouxsein ML, Canalis E, Sun H, Glatt V, Gundberg C, Cohen P, Hwang D, Boisclair Y, Leroith D, Rosen CJ. The ternary IGF complex influences postnatal bone acquisition and the skeletal response to intermittent parathyroid hormone. J Endocrinol. 2006; 189: 289 – 99.en_US
dc.identifier.citedreferenceElis S, Courtland HW, Wu J, Fritton JC, Sun H, Rosen CJ, Yakar S. Elevated serum IGF‐1 levels synergize PTH action on the skeleton only when the tissue IGF‐1 axis is intact. J Bone Miner Res. 2010; 25: 2051 – 8.en_US
dc.identifier.citedreferenceColes JM, Zhang L, Blum JJ, Warman ML, Jay GD, Guilak F, Zauscher S. Loss of cartilage structure, stiffness, and frictional properties in mice lacking PRG4. Arthritis Rheum. 2010; 62: 1666 – 74.en_US
dc.identifier.citedreferenceLinkhart TA, Mohan S. Parathyroid hormone stimulates release of insulin‐like growth factor‐I (IGF‐I) and IGF‐II from neonatal mouse calvaria in organ culture. Endocrinology. 1989; 125: 1484 – 91.en_US
dc.identifier.citedreferenceLazowski DA, Fraher LJ, Hodsman A, Steer B, Modrowski D, Han VK. Regional variation of insulin‐like growth factor‐I gene expression in mature rat bone and cartilage. Bone. 1994; 15: 563 – 76.en_US
dc.identifier.citedreferenceSjögren K, Liu JL, Blad K, Skrtic S, Vidal O, Wallenius V, Leroith D, Tornell J, Isaksson OG, Jansson JO, Ohlsson C. Liver‐derived insulin‐like growth factor I (IGF‐I) is the principal source of IGF‐I in blood but is not required for postnatal body growth in mice. Proc Natl Acad Sci U S A. 1999; 96: 7088 – 92.en_US
dc.identifier.citedreferencePfeilschifter J, Laukhuf F, Muller‐Beckmann B, Blum WF, Pfister T, Ziegler R. Parathyroid hormone increases the concentration of insulin‐like growth factor‐I and transforming growth factor beta 1 in rat bone. J Clin Invest. 1995; 96: 767 – 74.en_US
dc.identifier.citedreferenceMontero A, Okada Y, Tomita M, Ito M, Tsurukami H, Nakamura T, Doetschman T, Coffin JD, Hurley MM. Disruption of the fibroblast growth factor‐2 gene results in decreased bone mass and bone formation. J Clin Invest. 2000; 105: 1085 – 93.en_US
dc.identifier.citedreferenceSabbieti MG, Agas D, Xiao L, Marchetti L, Coffin JD, Doetschman T, Hurley MM. Endogenous FGF‐2 is critically important in PTH anabolic effects on bone. J Cell Physiol. 2009; 219: 143 – 51.en_US
dc.identifier.citedreferenceSchumacher BL, Hughes CE, Kuettner KE, Caterson B, Aydelotte MB. Immunodetection and partial cDNA sequence of the proteoglycan, superficial zone protein, synthesized by cells lining synovial joints. J Orthop Res. 1999; 17: 110 – 20.en_US
dc.identifier.citedreferenceMerberg DM, Fitz L, Temple P, Giannotti J, Murtha P, Fitzgerald M, Scaltreto H, Kelleher K, Preissner K, Kriz R, Jacobs K, Turner K. A comparison of vitronectin and megakaryocyte stimulating factor. In: Preissner KT, Kost C, Wegerhoff J, Mosher DF, editors. Biology of vitronectins and their receptors. Philadelphia: Elsevier; 1992. p. 45 – 53.en_US
dc.identifier.citedreferenceKobayashi T, Chung UI, Schipani E, Starbuck M, Karsenty G, Katagiri T, Goad DL, Lanske B, Kronenberg HM. PTHrP and Indian hedgehog control differentiation of growth plate chondrocytes at multiple steps. Development. 2002; 129: 2977 – 86.en_US
dc.identifier.citedreferenceNagai H, Tsukuda R, Mayahara H. Effects of basic fibroblast growth factor (bFGF) on bone formation in growing rats. Bone. 1995; 16: 367 – 73.en_US
dc.identifier.citedreferenceLiang H, Pun S, Wronski TJ. Bone anabolic effects of basic fibroblast growth factor in ovariectomized rats. Endocrinology. 1999; 140: 5780 – 8.en_US
dc.identifier.citedreferenceNakamura T, Hanada K, Tamura M, Shibanushi T, Nigi H, Tagawa M, Fukumoto S, Matsumoto T. Stimulation of endosteal bone formation by systemic injections of recombinant basic fibroblast growth factor in rats. Endocrinology. 1995; 136: 1276 – 84.en_US
dc.identifier.citedreferenceGonzalez AM, Buscaglia M, Ong M, Baird A. Distribution of basic fibroblast growth factor in the 18‐day rat fetus: localization in the basement membranes of diverse tissues. J Cell Biol. 1990; 110: 753 – 65.en_US
dc.identifier.citedreferenceBrunner G, Gabrilove J, Rifkin DB, Wilson EL. Phospholipase C release of basic fibroblast growth factor from human bone marrow cultures as a biologically active complex with a phosphatidylinositol‐anchored heparan sulfate proteoglycan. J Cell Biol. 1991; 114: 1275 – 83.en_US
dc.identifier.citedreferenceBrunner G, Nguyen H, Gabrilove J, Rifkin DB, Wilson EL. Basic fibroblast growth factor expression in human bone marrow and peripheral blood cells. Blood. 1993; 81: 631 – 8.en_US
dc.identifier.citedreferenceThomson BM, Bennett J, Dean V, Triffitt J, Meikle MC, Loveridge N. Preliminary characterization of porcine bone marrow stromal cells: skeletogenic potential, colony‐forming activity, and response to dexamethasone, transforming growth factor beta, and basic fibroblast growth factor. J Bone Miner Res. 1993; 8: 1173 – 83.en_US
dc.identifier.citedreferenceLong MW, Robinson JA, Ashcraft EA, Mann KG. Regulation of human bone marrow‐derived osteoprogenitor cells by osteogenic growth factors. J Clin Invest. 1995; 95: 881 – 7.en_US
dc.identifier.citedreferenceChow NH, Cheng KS, Lin PW, Chan SH, Su WC, Sun YN, Lin XZ. Expression of fibroblast growth factor‐1 and fibroblast growth factor‐2 in normal liver and hepatocellular carcinoma. Digest Dis Sci. 1998; 43: 2261 – 6.en_US
dc.identifier.citedreferenceHioki O, Minemura M, Shimizu Y, Kasii Y, Nishimori H, Takahara T, Higuchi K, Yoshitake Y, Nishikawa K, Watanabe A. Expression and localization of basic fibroblast growth factor (bFGF) in the repair process of rat liver injury. J Hepatol. 1996; 24: 217 – 24.en_US
dc.identifier.citedreferenceHurley MM, Yao M, Lane NE. Changes in serum fibroblast growth factor 2 in patients with glucocorticoid‐induced osteoporosis treated with human parathyroid hormone (1–34). Osteoporosis Int. 2005; 16: 2080 – 4.en_US
dc.identifier.citedreferenceMayahara H, Ito T, Nagai H, Miyajima H, Tsukuda R, Taketomi S, Mizoguchi J. Kat. In vivo stimulation of endosteal bone formation by basic fibroblast growth factor in rats. Growth Factors. 1993; 9: 73 – 80.en_US
dc.identifier.citedreferenceBagi CM, Mecham M, Weiss J, Miller SC. Comparative morphometric changes in rat cortical bone following ovariectomy and/or immobilization. Bone. 1993; 14: 877 – 83.en_US
dc.identifier.citedreferenceLi XJ, Jee WS. Adaptation of diaphyseal structure to aging and decreased mechanical loading in the adult rat: a densitometric and histomorphometric study. Anat Rec. 1991; 229: 291 – 7.en_US
dc.identifier.citedreferenceTurner RT, Lotinun S, Hefferan TE, Morey‐Holton E. Disuse in adult male rats attenuates the bone anabolic response to a therapeutic dose of parathyroid hormone. J Appl Physiol. 2006; 101: 881 – 6.en_US
dc.identifier.citedreferenceHalloran BP, Bikle DD, Haris J, Tanner S, Curren T, Morey‐Holton E. Regional responsiveness of the tibia to intermittent administration of parathyroid hormone as affected by skeletal unloading. J Bone Miner Res. 1997; 12: 1068 – 74.en_US
dc.identifier.citedreferenceMoriyama I, Iwamoto J, Takeda T, Toyama Y. Comparative effects of intermittent administration of human parathyroid hormone (1–34) on cancellous and cortical bone loss in tail‐suspended and sciatic neurectomized young rats. J Orthop Sci. 2002; 7: 379 – 85.en_US
dc.identifier.citedreferenceLi XJ, Jee WS, Chow SY, Woodbury DM. Adaptation of cancellous bone to aging and immobilization in the rat: a single photon absorptiometry and histomorphometry study. Anat Rec. 1990; 227: 12 – 24.en_US
dc.identifier.citedreferenceChen MM, Jee WS, Ke HZ, Lin BY, Li QN, Li XJ. Adaptation of cancellous bone to aging and immobilization in growing rats. Anat Rec. 1992; 234: 317 – 34.en_US
dc.identifier.citedreferenceLi M, Jee WS, Ke HZ, Liang XG, Lin BY, Ma YF, Setterberg RB. Prostaglandin E2 restores cancellous bone to immobilized limb and adds bone to overloaded limb in right hindlimb immobilization rats. Bone. 1993; 14: 283 – 8.en_US
dc.identifier.citedreferenceMa YF, Jee WS, Ke HZ, Lin BY, Liang XG, Li M, Yamamoto N. Human parathyroid hormone‐(1–38) restores cancellous bone to the immobilized, osteopenic proximal tibial metaphysis in rats. J Bone Miner Res. 1995; 10: 496 – 505.en_US
dc.identifier.citedreferenceTurner RT, Evans GL, Cavolina JM, Halloran B, Morey‐Holton E. Programmed administration of parathyroid hormone increases bone formation and reduces bone loss in hindlimb‐unloaded ovariectomized rats. Endocrinology. 1998; 139: 4086 – 91.en_US
dc.identifier.citedreferenceMitnick MA, Grey A, Masiukiewicz U, Bartkiewicz M, Rios‐Velez L, Friedman S, Xu L, Horowitz MC, Insogna K. Parathyroid hormone induces hepatic production of bioactive interleukin‐6 and its soluble receptor. Am J Physiol Endocrinol Metab. 2001; 280: E405 – 12.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
508_ftp.pdf
Size:
870.1KB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.