Intermittent PTH Administration Increases Bone-Specific Blood Vessels and Surrounding Stromal Cells in Murine Long Bones.


Journal

Calcified tissue international
ISSN: 1432-0827
Titre abrégé: Calcif Tissue Int
Pays: United States
ID NLM: 7905481

Informations de publication

Date de publication:
03 2021
Historique:
received: 07 07 2020
accepted: 29 10 2020
pubmed: 11 11 2020
medline: 30 7 2021
entrez: 10 11 2020
Statut: ppublish

Résumé

To verify whether PTH acts on bone-specific blood vessels and on cells surrounding these blood vessels, 6-week-old male mice were subjected to vehicle (control group) or hPTH [1-34] (20 µg/kg/day, PTH group) injections for 2 weeks. Femoral metaphyses were used for histochemical and immunohistochemical studies. In control metaphyses, endomucin-positive blood vessels were abundant, but αSMA-reactive blood vessels were scarce. In the PTH-administered mice, the lumen of endomucin-positive blood vessels was markedly enlarged. Moreover, many αSMA-positive cells were evident near the blood vessels, and seemed to derive from those vessels. These αSMA-positive cells neighboring the blood vessels showed features of mesenchymal stromal cells, such as immunopositivity for c-kit and tissue nonspecific alkaline phosphatase (TNALP). Thus, PTH administration increased the population of perivascular/stromal cells positive for αSMA and c-kit, which were likely committed to the osteoblastic lineage. To understand the cellular events that led to increased numbers and size of bone-specific blood vessels, we performed immunohistochemical studies for PTH/PTHrP receptor and VEGF. After PTH administration, PTH/PTHrP receptor, VEGF and its receptor flk-1 were consistently identified in both osteoblasts and blood vessels (endothelial cells and surrounding perivascular cells). Our findings suggest that exogenous PTH increases the number and size of bone-specific blood vessels while fostering perivascular/stromal cells positive for αSMA/TNALP/c-kit.

Identifiants

pubmed: 33170307
doi: 10.1007/s00223-020-00776-2
pii: 10.1007/s00223-020-00776-2
doi:

Substances chimiques

Parathyroid Hormone 0
Receptor, Parathyroid Hormone, Type 1 0
Vascular Endothelial Growth Factor A 0
vascular endothelial growth factor A, mouse 0
Proto-Oncogene Proteins c-kit EC 2.7.10.1
Vascular Endothelial Growth Factor Receptor-2 EC 2.7.10.1
ALPL protein, mouse EC 3.1.3.1
Alkaline Phosphatase EC 3.1.3.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

391-406

Références

Schweser KM, Crist BD (2017) Osteoporosis: a discussion on the past 5 years. Curr Rev Musculoskelet Med 10:265–274
doi: 10.1007/s12178-017-9410-y
Orwoll E, Scheele W, Paul S, Adami S, Syversen U, Diez-Perez A, Kaufman JM, Clancy AD, Gaich GA (2003) The effect of teriparatide [human parathyroid hormone (1–34)] therapy on bone density in men with osteoporosis. J Bone Miner Res 18:9–17
doi: 10.1359/jbmr.2003.18.1.9
Cosman F, Hattersley G, Hu MY, Williams GC, Fitzpatrick LA, Black DM (2017) Effects of abaloparatide-SC on fractures and bone mineral density in subgroups of postmenopausal women with osteoporosis and varying baseline risk factors. J Bone Miner Res 32(1):17–23
doi: 10.1002/jbmr.2991
Skripitz R, Aspenberg P (2004) Parathyroid hormone–a drug for orthopedic surgery? Acta Orthop Scand 75:654–662
doi: 10.1080/00016470410004012
Moreira CA, Fitzpatrick LA, Wang Y, Recker RR (2017) Effects of abaloparatide-SC (BA058) on bone histology and histomorphometry: the ACTIVE phase 3 trial. Bone 97:314–319
doi: 10.1016/j.bone.2016.11.004
Luiz de Freitas PH, Li M, Ninomiya T, Nakamura M, Ubaidus S, Oda K, Udagawa N, Maeda T, Takagi R, Amizuka N (2009) Intermittent PTH administration stimulates pre-osteoblastic proliferation without leading to enhanced bone formation in osteoclast-less c-fos(-/-) mice. J Bone Miner Res 24:1586–1597
doi: 10.1359/jbmr.090413
Yamamoto T, Hasegawa T, Sasaki M, Hongo H, Tsuboi K, Shimizu T, Ohta M, Haraguchi M, Takahata T, Oda K, Freitas PHL, Takakura A, Takao-Kawabata R, Isogai Y, Amizuka N (2016) Frequency of teriparatide administration affects the histological pattern of bone formation in young adult male mice. Endocrinology 157:2604–2620
doi: 10.1210/en.2015-2028
Dhillon RS, Xie C, Tyler W, Calvi LM, Awad HA, Zuscik MJ, O’Keefe RJ, Schwarz EM (2013) PTH-enhanced structural allograft healing is associated with decreased angiopoietin-2-mediated arteriogenesis, mast cell accumulation, and fibrosis. J Bone Miner Res 28(3):586–597
doi: 10.1002/jbmr.1765
Jiang X, Xu C, Shi H, Cheng Q (2019) PTH 1–34 improves bone healing by promoting angiogenesis and facilitating MSCs migration and differentiation in a stabilized fracture mouse model. PLoS ONE 14(12):e0226163
doi: 10.1371/journal.pone.0226163
Kusumbe AP, Ramasamy SK, Adams RH (2014) Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature 507:323–328
doi: 10.1038/nature13145
Ramasamy SK, Kusumbe AP, Wang L, Adams RH (2014) Endothelial Notch activity promotes angiogenesis and osteogenesis in bone. Nature 507:376–380
doi: 10.1038/nature13146
Wang HU, Chen ZF, Anderson DJ (1998) Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93(5):741–753
doi: 10.1016/S0092-8674(00)81436-1
Rundle CH, Xing W, Lau KW, Mohan S (2016) Bidirectional ephrin signaling in bone. Osteoporos Sarcopenia 2:65–76
doi: 10.1016/j.afos.2016.05.002
Zhao C, Irie N, Takada Y, Shimoda K, Miyamoto T, Nishiwaki T, Suda T, Matsuo K (2006) Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab 4:111–121
doi: 10.1016/j.cmet.2006.05.012
Ramasamy SK (2017) Structure and functions of blood vessels and vascular niches in bone. Stem Cells Int 2017:5046953
doi: 10.1155/2017/5046953
Armulik A, Genove G, Betsholtz C (2011) Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 21:193–215
doi: 10.1016/j.devcel.2011.07.001
Sivaraj KK, Adams RH (2016) Blood vessel formation and function in bone. Development 143:2706–2715
doi: 10.1242/dev.136861
Aizman I, Holland WS, Yang C, Bates D (2016) alphaSMA expression in large colonies of colony-forming units-fibroblast as an early predictor of bone marrow MSC expandability. Cell Med 8:79–85
doi: 10.3727/215517916X693357
Hosoya A, Nakamura H, Ninomiya T, Yoshiba K, Yoshiba N, Nakaya H, Wakitani S, Yamada H, Kasahara E, Ozawa H (2006) Immunohistochemical localization of alpha-smooth muscle actin during rat molar tooth development. J Histochem Cytochem 54(12):1371–1378
doi: 10.1369/jhc.6A6980.2006
Matthews BG, Grcevic D, Wang L, Hagiwara Y, Roguljic H, Joshi P, Shin DG, Adams DJ, Kalajzic I (2014) Analysis of alphaSMA-labeled progenitor cell commitment identifies notch signaling as an important pathway in fracture healing. J Bone Miner Res 29:1283–1294
doi: 10.1002/jbmr.2140
Kusumbe AP, Ramasamy SK, Itkin T, Mae MA, Langen UH, Betsholtz C, Lapidot T, Adams RH (2016) Age-dependent modulation of vascular niches for haematopoietic stem cells. Nature 532:380–384
doi: 10.1038/nature17638
Kunisaki Y, Bruns I, Scheiermann C, Ahmed J, Pinho S, Zhang D, Mizoguchi T, Wei Q, Lucas D, Ito K, Mar JC, Bergman A, Frenette PS (2013) Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 502:637–643
doi: 10.1038/nature12612
Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, Scadden DT, Ma’ayan A, Enikolopov GN, Frenette PS (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466:829–834
doi: 10.1038/nature09262
Root SH, Wee NK-Y, Novak S, Rosen CJ, Baron R, Matthews BG, Kalajzic I (2020) Perivascular osteoprogenitors are associated wih transcortical channels of long bones. Stem Cell 38:769–781
doi: 10.1002/stem.3159
Hasegawa T, Yamamoto T, Sakai S, Miyamoto Y, Hongo H, Qiu Z, Abe M, Takeda S, Oda K, de Freitas PHL, Li M, Endo K, Amizuka N (2019) Histological effects of the combined administration of eldecalcitol and a parathyroid hormone in the metaphyseal trabeculae of ovariectomized rats. J Histochem Cytochem 67(3):169–184
doi: 10.1369/0022155418806865
Oda K, Amaya Y, Fukushi-Irié M, Kinameri Y, Ohsuye K, Kubota I, Fujimura S, Kobayashi J (1999) A general method for rapid purification of soluble versions of glycosylphosphatidylinositol-anchored proteins expressed in insect cells: an application for human tissue-nonspecific alkaline phosphatase. J Biochem 126:694–699
doi: 10.1093/oxfordjournals.jbchem.a022505
Deng W (2010) Mesenchymal stem cells express C-kit. Circ Res 107(10):e17
doi: 10.1161/CIRCRESAHA.110.230961
Amizuka N, Lee HS, Kwan MY, Arazani A, Warshawsky H, Hendy GN, Ozawa H, White JH, Goltzman D (1997) Cell-specific expression of the parathyroid hormone (PTH)/PTH-related peptide receptor gene in kidney from kidney-specific and ubiquitous promoters. Endocrinology 138(1):469–481
doi: 10.1210/endo.138.1.4845
Jiang L, Zhang W, Wei L, Zhou Q, Yang G, Qian N, Tang Y, Gao Y, Jiang X (2018) Early effects of parathyroid hormone on vascularized bone regeneration and implant osseointegration in aged rats. Biomaterials 179:15–28
doi: 10.1016/j.biomaterials.2018.06.035
Pang PK, Tenner TE Jr, Yee JA, Yang M, Janssen HF (1980) Hypotensive action of parathyroid hormone preparations on rats and dogs. Proc Natl Acad Sci USA 77(1):675–678
doi: 10.1073/pnas.77.1.675
Nickols GA (1985) Increased cyclic AMP in cultured vascular smooth muscle cells and relaxation of aortic strips by parathyroid hormone. Eur J Pharmacol 116(1–2):137–144
doi: 10.1016/0014-2999(85)90194-3
Nickols GA, Metz MA, Cline WH Jr (1986) Endothelium-independent linkage of parathyroid hormone receptors of rat vascular tissue with increased adenosine 3’,5’-monophosphate and relaxation of vascular smooth muscle. Endocrinology 119(1):349–356
doi: 10.1210/endo-119-1-349
He DD, Tang XT, Dong W, Cui G, Peng G, Yin X, Chen Y, Jing N, Zhou BO (2020) C-kit expression distinguishes fetal from postnatal skeletal progenitors. Stem Cell Rep 14(4):614–630
doi: 10.1016/j.stemcr.2020.03.001
Portal-Nunez S, Lozano D, Esbrit P (2012) Role of angiogenesis on bone formation. Histol Histopathol 27:559–566
pubmed: 22419020
Grüneboom A, Hawwari I, Weidner D, Culemann S, Müller S, Henneberg S, Henneberg S, Brenzel A, Merz S, Bornemann L, Zec K, Wuelling M, Kling L, Hasenberg M, Voortmann S, Lang S, Baum W, Ohs A, Kraff O, Quick HH, Jäger M, Landgraeber S, Dudda M, Danuser R, Stein JV, Rohde M, Gelse K, Garbe AI, Adamczyk A, Westendorf AM, Hoffmann D, Christiansen S, Engel DR, Vortkamp A, Krönke G, Herrmann M, Kamradt T, Schett G, Hasenberg A, Gunzer M (2019) A network of trans-cortical capillaries as mainstay for blood circulation in long bones. Nat Metab 1:236–250
doi: 10.1038/s42255-018-0016-5
Marini M, Rosa I, Ibba-Manneschi L, Manetti M (2018) Telocytes in skeletal, cardiac and smooth muscle interstitium: morphological and functional aspects. Histol Histopathol 33:1151–1165
pubmed: 29693711

Auteurs

Shen Zhao (S)

National Clinical Research Center of Stomatology, Department of Endodontics, School of Medicine, Shanghai Key Laboratory of Stomatology & Shanghai Research Institute of Stomatology, Ninth People's Hospital, Shanghai Jiaotong University, Shanghai, China.
Developmental Biology of Hard Tissue, Graduate School of Dental Medicine, Faculty of Dental Medicine, Hokkaido University, Kita 13 Nishi 7 Kita-ku, Sapporo, 060-8586, Japan.
Oral and Maxillofacial Surgery, Graduate School of Dental Medicine, Faculty of Dental Medicine, Hokkaido University, Sapporo, Japan.

Tomoka Hasegawa (T)

Developmental Biology of Hard Tissue, Graduate School of Dental Medicine, Faculty of Dental Medicine, Hokkaido University, Kita 13 Nishi 7 Kita-ku, Sapporo, 060-8586, Japan. hasegawa@den.hokudai.ac.jp.

Hiromi Hongo (H)

Developmental Biology of Hard Tissue, Graduate School of Dental Medicine, Faculty of Dental Medicine, Hokkaido University, Kita 13 Nishi 7 Kita-ku, Sapporo, 060-8586, Japan.

Tomomaya Yamamoto (T)

Section of Dentistry, Camp Asaka, Japan Ground Self-Defense Forces, Tokyo, Japan.

Miki Abe (M)

Developmental Biology of Hard Tissue, Graduate School of Dental Medicine, Faculty of Dental Medicine, Hokkaido University, Kita 13 Nishi 7 Kita-ku, Sapporo, 060-8586, Japan.

Taiji Yoshida (T)

Developmental Biology of Hard Tissue, Graduate School of Dental Medicine, Faculty of Dental Medicine, Hokkaido University, Kita 13 Nishi 7 Kita-ku, Sapporo, 060-8586, Japan.

Mai Haraguchi (M)

Developmental Biology of Hard Tissue, Graduate School of Dental Medicine, Faculty of Dental Medicine, Hokkaido University, Kita 13 Nishi 7 Kita-ku, Sapporo, 060-8586, Japan.

Paulo Henrique Luiz de Freitas (PHL)

Department of Dentistry, Federal University of Sergipe, Lagarto, Brazil.

Minqi Li (M)

Shandong Provincial Key Laboratory of Oral Biomedicine, The School of Stomatology, Shandong University, Jinan, China.

Kanchu Tei (K)

Oral and Maxillofacial Surgery, Graduate School of Dental Medicine, Faculty of Dental Medicine, Hokkaido University, Sapporo, Japan.

Norio Amizuka (N)

Developmental Biology of Hard Tissue, Graduate School of Dental Medicine, Faculty of Dental Medicine, Hokkaido University, Kita 13 Nishi 7 Kita-ku, Sapporo, 060-8586, Japan.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH