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Citations to this article

Identification of haptoglobin as an angiogenic factor in sera from patients with systemic vasculitis.
M C Cid, … , A S Fauci, H K Kleinman
M C Cid, … , A S Fauci, H K Kleinman
Published March 1, 1993
Citation Information: J Clin Invest. 1993;91(3):977-985. https://doi.org/10.1172/JCI116319.
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Research Article Article has an altmetric score of 6

Identification of haptoglobin as an angiogenic factor in sera from patients with systemic vasculitis.

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Abstract

Angiogenesis is an important process in chronic inflammatory diseases. We observed that sera from patients with systemic vasculitis stimulated angiogenesis in an in vitro model using human umbilical vein endothelial cells cultured on a basement membrane (Matrigel) substrate. After 40% ammonium sulfate precipitation, angiogenic activity remained in the low molecular weight fraction and could be inactivated by heat. SDS-page of serum FPLC fractions exhibiting maximal angiogenic activity demonstrated two prominent species of 45 and 16-20 kD in patients' sera. These bands were much less apparent in sera obtained from control subjects. Amino-terminal sequencing of the 45-kD protein demonstrated that it was haptoglobin. Purified haptoglobin stimulated angiogenesis in a dose-dependent manner. The angiogenic activity of vasculitis patients' sera was partially inhibited by an antihaptoglobin antibody. Furthermore, serum haptoglobin levels in vasculitis patients correlated both with disease and angiogenic activity. Haptoglobin angiogenic activity was confirmed in two in vivo models using an implanted disc and a subcutaneous injection of basement membrane. Stimulation of angiogenesis is a newly recognized biological function of haptoglobin. The increased levels of haptoglobin found in chronic inflammatory conditions may play an important role in tissue repair. In systemic vasculitis, haptoglobin might also compensate for ischemia by promoting development of collateral vessels.

Authors

M C Cid, D S Grant, G S Hoffman, R Auerbach, A S Fauci, H K Kleinman

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C Murray, S Martin
2008
Improved Diagnosis of Pancreatic Adenocarcinoma Using Haptoglobin and Serum Amyloid A in a Panel Screen
MA Firpo, DZ Gay, SR Granger, CL Scaife, JA DiSario, KM Boucher, SJ Mulvihill
World Journal of Surgery 2008
Haptoglobin from psoriatic patients exhibits decreased activity in binding haemoglobin and inhibiting lecithin-cholesterol acyltransferase activity
L Cigliano, B Maresca, A Salvatore, M Nino, G Monfrecola, F Ayala, A Carlucci, RC Pugliese, C Pedone, P Abrescia
Journal of the European Academy of Dermatology and Venereology 2008
Structural Stabilization in Tetrameric or Polymeric Hemoglobin Determines Its Interaction with Endogenous Antioxidant Scavenger Pathways
PW Buehler, F Vallelian, MG Mikolajczyk, G Schoedon, T Schweizer, AI Alayash, DJ Schaer
Antioxidants & Redox Signaling 2008
The functional polymorphism of the hemoglobin-binding protein haptoglobin influences susceptibility to idiopathic Parkinson's disease
P Costa-Mallen, H Checkoway, A Zabeti, MJ Edenfield, PD Swanson, WT Longstreth, GM Franklin, T Smith-Weller, SM Sadrzadeh
American Journal of Medical Genetics Part B: Neuropsychiatric Genetics 2008
Haptoglobin, inflammation and disease
IK Quaye
Transactions of the Royal Society of Tropical Medicine and Hygiene 2008
Blood Proteins and Inflammation in the Horse
MV Crisman, WK Scarratt, KL Zimmerman
Veterinary Clinics of North America: Equine Practice 2008
Haptoglobin phenotype is not a predictor of recurrence free survival in high-risk primary breast cancer patients
MC Gast, H Tinteren, M Bontenbal, RQ van Hoesel, MA Nooij, S Rodenhuis, PN Span, VC Tjan-Heijnen, EG de Vries, N Harris, JW Twisk, JH Schellens, JH Beijnen
BMC Cancer 2008
Polymorphism of human haptoglobin and its clinical importance
VP de Wobeto, TR Zaccariotto, MF Sonati
Genetics and molecular biology 2008
Serum Haptoglobin Levels in Ocular Behçet Disease and Acute Phase Proteins in the Course of Behçet Disease
FN Yalçindağ, A YalçIndağ, O Çağlayan, Ö Özdemir
European journal of ophthalmology 2008
Heat Shock Proteins and the Brain: Implications for Neurodegenerative Diseases and Neuroprotection
AA Asea, IR Brown
2008
Angiogenesis Protocols
C Murray, S Martin
2008
Impairment of Angiogenic Activity in the Serum From Patients With Coronary Aneurysms Due to Kawasaki Disease
K Higashi, M Terai, H Hamada, T Honda, M Kanazawa, Y Kohno
Circulation Journal 2007
Haptoglobin and posttranslational glycan-modified derivatives as serum biomarkers for the diagnosis of nonsmall cell lung cancer
LF Hoagland, MJ Campa, EB Gottlin, JE Herndon, EF Patz
Cancer 2007
Haptoglobin: a review of the major allele frequencies worldwide and their association with diseases
K Carter, M Worwood
International Journal of Laboratory Hematology 2007
Protein Kinase C-delta Stimulates Haptoglobin Secretion
MK Oh, SJ Park, NH Kim, IS Kim
Journal of Biochemistry and molecular biology 2007
Pathophysiological Roles of ASK1-MAP Kinase Signaling Pathways
H Nagai, T Noguchi, K Takeda, H Ichijo
Journal of Biochemistry and molecular biology 2007
Proteomic analysis of ovomucoid hypersensitivity in mice by two-dimensional difference gel electrophoresis (2D-DIGE)
DJ Hobson, P Rupa, GJ Diaz, H Zhang, M Yang, Y Mine, PV Turner, GM Kirby
Food and Chemical Toxicology 2007
Serum vascular endothelial growth factor in cyanotic congenital heart disease functionally contributes to endothelial cell kinetics in vitro
H Hamada, R Ebata, K Higashi, S Tateno, K Niwa, T Honda, K Yasukawa, M Terai
International Journal of Cardiology 2007
Haptoglobin is degraded by iron in C57BL/6 mice: A possible link with endoplasmic reticulum stress
A Faye, G Ramey, M Foretz, S Vaulont
Blood Cells, Molecules, and Diseases 2007
Inflammation inhibitors were remarkably up-regulated in plasma of severe acute respiratory syndrome patients at progressive phase
J Wan, W Sun, X Li, W Ying, J Dai, X Kuai, H Wei, X Gao, Y Zhu, Y Jiang, X Qian, F He
PROTEOMICS 2006
Haptoglobin polymorphism in patients with preeclampsia
HT Depypere, MR Langlois, JR Delanghe, M Temmerman, M Dhont
Clinical Chemistry and Laboratory Medicine 2006
Altered proteome profiles in maternal plasma in pregnancies with fetal growth restriction
MB Gupta, MD Seferovic, S Liu, RJ Gratton, A Doherty-Kirby, GA Lajoie, VK Han
Clinical Proteomics 2006
Postoperative serum proteomic profiles may predict metastatic relapse in high-risk primary breast cancer patients receiving adjuvant chemotherapy
A Gonçalves, B Esterni, F Bertucci, R Sauvan, C Chabannon, M Cubizolles, VJ Bardou, G Houvenaegel, J Jacquemier, S Granjeaud, XY Meng, ET Fung, D Birnbaum, D Maraninchi, P Viens, JP Borg
Oncogene 2005
Staurosporine Promotes Endothelial Cell Assembly and FAK Phosphorylation During In Vitro Angiogenesis
ST Tarzami, SS Hsieh, MA Esterman, JP Singh
Journal of Cardiovascular Pharmacology 2005
Inflammatory C-reactive protein and cytokine levels in asymptomatic people with chronic spinal cord injury
F Frost, MJ Roach, I Kushner, P Schreiber
Archives of Physical Medicine and Rehabilitation 2005
Haptoglobin expression and activity during coronary collateralization
NL Lohr, DC Warltier, WM Chilian, D Weihrauch
American journal of physiology. Heart and circulatory physiology 2005
The bHLH TAL-1/SCL regulates endothelial cell migration and morphogenesis
M Lazrak, V Deleuze, D Noel, D Haouzi, E Chalhoub, C Dohet, I Robbins, D Mathieu
Journal of cell science 2004
Haptoglobin phenotype correlates with development of cardiac transplant vasculopathy
CG Densem, J Wassel, A Cooper, N Yonan, NH Brooks, B Keevil
The Journal of Heart and Lung Transplantation 2004
The comparative analysis of serum proteomes for the discovery of biomarkers for acute myeloid leukemia
JY Kwak, TZ Ma, MJ Yoo, BH Choi, HG Kim, SR Kim, CY Yim, YG Kwak
Experimental Hematology 2004
Regulation of haptoglobin gene expression in 3T3-L1 adipocytes by cytokines, catecholamines, and PPARγ
CO Nascimento, L Hunter, P Trayhurn
Biochemical and Biophysical Research Communications 2004
Données physiopathologiques
T Généreau, K Tiev, M Rabhi, M Baret, J Cabane
La Presse Médicale 2004
Haptoglobin polymorphism in breast cancer patients form Jordan
SM Awadallah, MF Atoum
Clinica Chimica Acta 2004
Expression of haptoglobin mRNA in the liver and oviduct during the oestrous cycle of cows (Bos taurus)
K Lavery, C Gabler, J Day, G Killian
Animal Reproduction Science 2004
Haptoglobin Phenotypes in Epilepsy
SM Sadrzadeh, Y Saffari, J Bozorgmehr
Clinical chemistry 2004
Haptoglobin directly affects T cells and suppresses T helper cell type 2 cytokine release
M Arredouani, P Matthijs, EV Hoeyveld, A Kasran, H Baumann, JL Ceuppens, E Stevens
Immunology 2003
Quantitative variations of the isoforms in haptoglobin 1-2 and 2-2 individual phenotypes
L Cigliano, MS Spagnuolo, P Abrescia
Archives of Biochemistry and Biophysics 2003
Acute-phase protein haptoglobin is a cell migration factor involved in arterial restructuring
DP de Kleijn, MB Smeets, PP Kemmeren, SK Lim, BJ van Middelaar, E Velema, A Schoneveld, G Pasterkamp, C Borst
The FASEB Journal 2002
Wiley Encyclopedia of Molecular Medicine
WT Morgan
Wiley Encyclopedia of Molecular Medicine 2002
Angiogenesis and chemokines in rheumatoid arthritis and other systemic inflammatory rheumatic diseases
E Bodolay, AE Koch, J Kim, G Szegedi, Z Szekanecz
Journal of Cellular and Molecular Medicine 2002
Upregulation of Haptoglobin in Reactive Astrocytes After Transient Forebrain Ischemia in Rats
MY Lee, SY Kim, JS Choi, IH Lee, YS Choi, JY Jin, SJ Park, KW Sung, MH Chun, IS Kim
Journal of Cerebral Blood Flow & Metabolism 2002
Haptoglobin: A major susceptibility gene for diabetic vascular complications
T Szafranek, S Marsh, AP Levy
Experimental and clinical cardiology 2002
Involvement of CCAAT/enhancer-binding protein α in haptoglobin gene expression by all-trans-retinoic acid
IH Lee, JH Lee, MJ Lee, SY Lee, IS Kim
Biochemical and Biophysical Research Communications 2002
Upregulation of Haptoglobin in Reactive Astrocytes after Transient Forebrain Ischemia in Rats
MY Lee, SY Kim, JS Choi, IH Lee, YS Choi, JY Jin, SJ Park, KW Sung, MH Chun, IS Kim
Journal of Cerebral Blood Flow & Metabolism 2002
Tissue and Serum Angiogenic Activity Is Associated With Low Prevalence of Ischemic Complications in Patients With Giant-Cell Arteritis
MC Cid, J Hernández-Rodríguez, MJ Esteban, M Cebrián, YS Gho, C Font, A Urbano-Márquez, JM Grau, HK Kleinman
Circulation 2002
The influence of vacuum-assisted closure on inflammatory tissue reactions in the postoperative course of ankle fractures
K Buttenschoen, W Fleischmann, U Haupt, L Kinzl, DC Buttenschoen
Foot and Ankle Surgery 2001
Obesity modulates the expression of haptoglobin in the white adipose tissue via TNFα: OBESITY INDUCES WAT HAPTOGLOBIN VIA TNFα
C Chiellini, A Bertacca, SE Novelli, CZ Görgün, A Ciccarone, A Giordano, H Xu, A Soukas, M Costa, D Gandini, R Dimitri, P Bottone, P Cecchetti, E Pardini, L Perego, R Navalesi, F Folli, L Benzi, S Cinti, JM Friedman, GS Hotamisligil, M Maffei
Journal of Cellular Physiology 2001
Social isolation stress augments angiogenesis induced by colon 26-L5 carcinoma cells in mice
W Wu, J Murata, K Murakami, T Yamaura, K Hayashi, I Saiki
Clinical & Experimental Metastasis 2001
Angiogenèse : mécanismes généraux et implications au cours de la polyarthrite rhumatoïde
AJ Weber, MD Bandt
Revue du Rhumatisme 2000
Pulmonary Expression of the Human Haptoglobin Gene
F Yang, AJ Ghio, DC Herbert, FJ Weaker, CA Walter, JJ Coalson
American journal of respiratory cell and molecular biology 2000
Nosocomial Pneumonia
UL Specks
Nosocomial Pneumonia 2000
Translocation of Endotoxin and Acute-Phase Proteins in Malleolar Fractures:
K Buttenschoen, W Fleischmann, U Haupt, L Kinzl, DC Buttenschoen
The Journal of trauma 2000
Haptoglobin polymorphism and peripheral arterial occlusive disease
J Delanghe, M Langlois, D Duprez, MD Buyzere, D Clement
Atherosclerosis 1999
Arterial wall injury in giant cell arteritis
CM Weyand, JJ Goronzy
Arthritis & Rheumatism 1999
Acute-Phase Proteins and Other Systemic Responses to Inflammation
FH Epstein, C Gabay, I Kushner
New England Journal of Medicine 1999
Regulation of Angiogenin Expression in Human HepG2 Hepatoma Cells by Mediators of the Acute-Phase Response
SJ Verselis, KA Olson, JW Fett
Biochemical and Biophysical Research Communications 1999
Detection of Haptoglobin in the High-Density Lipoprotein and the Very High-Density Lipoprotein Fractions from Sera of Calves with Experimental Pneumonia and Cows with Naturally Occurring Fatty Liver
N KATOH, H NAKAGAWA
Journal of Veterinary Medical Science 1999
Identification of laminin α1 and β1 chain peptides active for endothelial cell adhesion, tube formation, and aortic sprouting
KM Malinda, M Nomizu, M Chung, M Delgado, Y Kuratomi, Y Yamada, HK Kleinman, ML Ponce
The FASEB Journal 1999
Inhibition by vasoactive intestinal polypeptide (VIP) of angiogenesis induced by murine Colon 26-L5 carcinoma cells metastasized in liver
M Ogasawara, J Murata, Y Kamitani, K Hayashi, I Saiki
Clinical & Experimental Metastasis 1999
Effects of acanthoic acid on TNF-alpha gene expression and haptoglobin synthesis
HS Kang, HK Song, JJ Lee, KH Pyun, I Choi
Mediators of Inflammation 1998
Diabetes
T Mandrup-Poulsen
BMJ (Clinical research ed.) 1998
Cloning and Sequencing of cDNA Encoding Haptoglobin, an Acute Phase Protein in Syrian Hamster, Mesacricetus auratus
K Yamamoto, I Matsui, T Nakatani, K Matsuura, H Sinohara
Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 1998
Association between strong inflammatory response and low risk of developing visual loss and other cranial ischemic complications in giant cell (temporal) arteritis
MC Cid, C Font, J Oristrell, A de la Sierra, B Coll-Vinent, A Lpez-Soto, J Vilaseca, A Urbano-Mrquez, JM Grau
Arthritis & Rheumatism 1998
Increased Susceptibility in Hp Knockout Mice During Acute Hemolysis
SK Lim, H Kim, SK Lim, A bin Ali, YK Lim, Y Wang, SM Chong, F Costantini, H Baumman
Blood 1998
Tissue, temporal and inducible expression pattern of haptoglobin in mice
J D'Armiento, SS Dalal, K Chada
Gene 1997
Von Willebrand factor in the outcome of temporal arteritis
MC Cid, J Monteagudo, J Oristrell, J Vilaseca, L Pallares, R Cervera, C Font, J Font, M Ingelmo, A Urbano-Marquez
Annals of the rheumatic diseases 1996
The acute phase response and the hematopoietic system: the role of cytokines
JE Trey, I Kushner
Critical Reviews in Oncology/Hematology 1995
Human interferon-inducible protein 10 is a potent inhibitor of angiogenesis in vivo
AL Angiolillo, C Sgadari, DD Taub, F Liao, JM Farber, S Maheshwari, HK Kleinman, GH Reaman, G Tosato
Journal of Experimental Medicine 1995
Expression of Vascular Endothelial Growth Factor From a Defective Herpes Simplex Virus Type 1 Amplicon Vector Induces Angiogenesis in Mice
EA Mesri, HJ Federoff, M Brownlee
Circulation research 1995
Angiogenesis: mechanistic insights, neovascular diseases, and therapeutic prospects
EJ Battegay
Journal of Molecular Medicine 1995
Immunopathogenesis and Treatment of Systemic Vasculitis
PW Mathieson
Clinical immunotherapeutics 1994
The acute phase response: General aspects
I Kushner, DL Rzewnicki
Baillière's Clinical Rheumatology 1994
International Review of Cytology
RA Miller
International Review of Cytology 1991
Determination of haptoglobin genotype in an Iranian population with idiopathic generalized epilepsy
Sukaina Al-balaghee, Zeinab Al-balaghee, Ashraf Shabani, Parinaz Ghadam, Mojgan Bandehpour, Ali Askari Mehr, Bahram Kazemi
Reports of Biochemistry & Molecular Biology

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