High-phytate/low-calcium diet is a risk factor for crystal nephropathies, renal phosphate wasting, and bone loss

Phosphate overload contributes to mineral bone disorders associated with crystal nephropathies. Phytate, the major form of phosphorus in plant seeds, is known as an indigestible and negligible in humans. However, the mechanism and adverse effects of high-phytate intake on Ca2+ and phosphate absorption and homeostasis are unknown. Here we show that excessive intake of phytate with a low-Ca2+ diet fed to rats contributed to the development of crystal nephropathies, renal phosphate wasting, and bone loss through tubular dysfunction secondary to dysregulation of intestinal calcium and phosphate absorption. Moreover, Ca2+ supplementation alleviated the detrimental effects of excess dietary phytate on bone and kidney through excretion of undigested Ca2+-phytate, which prevented a vicious cycle of intestinal phosphate overload and renal phosphate wasting while improving intestinal Ca2+ bioavailability. Thus, we demonstrate that phytate is digestible without a high-Ca2+ diet and a risk factor for phosphate overloading and developing crystal nephropathies and bone disease.

[1]  R. Pearse,et al.  Elevated urea-to-creatinine ratio provides a biochemical signature of muscle catabolism and persistent critical illness after major trauma , 2019, Intensive Care Medicine.

[2]  Xianlin Han,et al.  SREBP-1a–stimulated lipid synthesis is required for macrophage phagocytosis downstream of TLR4-directed mTORC1 , 2018, Proceedings of the National Academy of Sciences.

[3]  J. Cha,et al.  Increased intracellular Ca2+ concentrations prevent membrane localization of PH domains through the formation of Ca2+-phosphoinositides , 2017, Proceedings of the National Academy of Sciences.

[4]  Mary B Leonard,et al.  Executive summary of the 2017 KDIGO Chronic Kidney Disease-Mineral and Bone Disorder (CKD-MBD) Guideline Update: what's changed and why it matters. , 2017, Kidney international.

[5]  H. Anders,et al.  Crystal nephropathies: mechanisms of crystal-induced kidney injury , 2017, Nature Reviews Nephrology.

[6]  G. Cheon,et al.  Impaired phagocytosis of apoptotic cells causes accumulation of bone marrow-derived macrophages in aged mice , 2017, BMB reports.

[7]  F. Paccaud,et al.  Fibroblast growth factor 23 and markers of mineral metabolism in individuals with preserved renal function. , 2016, Kidney international.

[8]  M. Billah,et al.  Dietary phytate intake inhibits the bioavailability of iron and calcium in the diets of pregnant women in rural Bangladesh: a cross-sectional study , 2016, BMC Nutrition.

[9]  Shery Jacob,et al.  A simple practice guide for dose conversion between animals and human , 2016, Journal of basic and clinical pharmacy.

[10]  E. Humer,et al.  Phytate in pig and poultry nutrition. , 2015, Journal of animal physiology and animal nutrition.

[11]  R. Unwin,et al.  What is nephrocalcinosis? , 2015, Kidney international.

[12]  C. Brearley,et al.  A Bacterial Homolog of a Eukaryotic Inositol Phosphate Signaling Enzyme Mediates Cross-kingdom Dialog in the Mammalian Gut , 2014, Cell reports.

[13]  M. Kuro-o Klotho, phosphate and FGF-23 in ageing and disturbed mineral metabolism , 2013, Nature Reviews Nephrology.

[14]  W. Xia,et al.  FGF23 and Phosphate Wasting Disorders , 2013, Bone Research.

[15]  R. Marwaha,et al.  Role of calcium deficiency in development of nutritional rickets in Indian children: a case control study. , 2012, The Journal of clinical endocrinology and metabolism.

[16]  J. Muñoz-Castañeda,et al.  Calcium deficiency reduces circulating levels of FGF23. , 2012, Journal of the American Society of Nephrology : JASN.

[17]  C. Shang,et al.  Quantifying phytate in dairy digesta and feces: alkaline extraction and high-performance ion chromatography. , 2012, Journal of dairy science.

[18]  Rinaldo Bellomo,et al.  The meaning of the blood urea nitrogen/creatinine ratio in acute kidney injury , 2012, Clinical kidney journal.

[19]  D. Milliner,et al.  Genetic determinants of urolithiasis , 2012, Nature Reviews Nephrology.

[20]  Pedagógia,et al.  Cross Sectional Study , 2019 .

[21]  J. S. Radcliffe,et al.  Vegetarian compared with meat dietary protein source and phosphorus homeostasis in chronic kidney disease. , 2011, Clinical journal of the American Society of Nephrology : CJASN.

[22]  T. Oh,et al.  β-propeller phytase hydrolyzes insoluble Ca(2+)-phytate salts and completely abrogates the ability of phytate to chelate metal ions. , 2010, Biochemistry.

[23]  K. Becker,et al.  Dietary roles of phytate and phytase in human nutrition: A review , 2010 .

[24]  Florian Kronenberg,et al.  Emerging risk factors and markers of chronic kidney disease progression , 2009, Nature Reviews Nephrology.

[25]  M. Razzaque,et al.  The FGF23–Klotho axis: endocrine regulation of phosphate homeostasis , 2009, Nature Reviews Endocrinology.

[26]  Chin A Modern Perspective , 2009 .

[27]  B. Gérard,et al.  NHERF1 mutations and responsiveness of renal parathyroid hormone. , 2008, The New England journal of medicine.

[28]  M. Schell,et al.  Do mammals make all their own inositol hexakisphosphate? , 2008, The Biochemical journal.

[29]  E. Ferguson,et al.  The concentrations of iron, calcium, zinc and phytate in cereals and legumes habitually consumed by infants living in East Lombok, Indonesia , 2007 .

[30]  V. Raboy,et al.  The ABCs of low-phytate crops , 2007, Nature Biotechnology.

[31]  P. Reynolds,et al.  Avian multiple inositol polyphosphate phosphatase is an active phytase that can be engineered to help ameliorate the planet's "phosphate crisis". , 2006, Journal of biotechnology.

[32]  R. Lifton,et al.  Wnk4 controls blood pressure and potassium homeostasis via regulation of mass and activity of the distal convoluted tubule , 2006, Nature Genetics.

[33]  T. Oh,et al.  Ca2+-inositol phosphate chelation mediates the substrate specificity of β-propeller phytase , 2006 .

[34]  Y. Okazaki,et al.  Effect of Dietary Level of Phytic Acid on Hepatic and Serum Lipid Status in Rats Fed a High-sucrose Diet , 2004, Bioscience, biotechnology, and biochemistry.

[35]  J. Phillips,et al.  Transgenic mice expressing bacterial phytase as a model for phosphorus pollution control , 2001, Nature Biotechnology.

[36]  J. Borzelleca,et al.  Comparison of AIN-76A and AIN-93G diets: a 13-week study in rats. , 2001, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[37]  V. Raboy Low-phytic-acid Grains , 2000 .

[38]  Joseph C. Shope,et al.  Intracellular delivery of phosphoinositides and inositol phosphates using polyamine carriers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[39]  N. Tandon,et al.  Prevalence and significance of low 25-hydroxyvitamin D concentrations in healthy subjects in Delhi. , 2000, The American journal of clinical nutrition.

[40]  Nam-Chul Ha,et al.  Crystal structures of a novel, thermostable phytase in partially and fully calcium-loaded states , 2000, Nature Structural Biology.

[41]  T. Martin,et al.  Tumor Necrosis Factor (cid:97) Stimulates Osteoclast Differentiation by a Mechanism Independent of the ODF/RANKL–RANK Interaction , 2022 .

[42]  S. Morony,et al.  OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis , 1999, Nature.

[43]  D. Lacey,et al.  Osteoprotegerin Ligand Is a Cytokine that Regulates Osteoclast Differentiation and Activation , 1998, Cell.

[44]  J. Pettifor Privational rickets: a modern perspective. , 1994, Journal of the Royal Society of Medicine.

[45]  B. Cooper,et al.  Phytase activity in the human and rat small intestine. , 1994, Gut.

[46]  J. M. Forbes,et al.  The voluntary intake of hay and silage by lactating cows in response to ruminal infusion of acetate or propionate, or both, with or without distension of the rumen by a balloon , 1993, British Journal of Nutrition.

[47]  A. Shamsuddin,et al.  [3H]phytic acid (inositol hexaphosphate) is absorbed and distributed to various tissues in rats. , 1993, The Journal of nutrition.

[48]  M. Calvo,et al.  Elevated secretion and action of serum parathyroid hormone in young adults consuming high phosphorus, low calcium diets assembled from common foods. , 1988, The Journal of clinical endocrinology and metabolism.

[49]  L. Thompson,et al.  Phytic acid and calcium affect the in vitro rate of navy bean starch digestion and blood glucose response in humans. , 1987, The American journal of clinical nutrition.

[50]  R. Reynolds,et al.  Phytate:zinc and phytate X calcium:zinc millimolar ratios in self-selected diets of Americans, Asian Indians, and Nepalese. , 1987, Journal of the American Dietetic Association.

[51]  V. Young,et al.  Metabolism of 14C-phytate in rats: effect of low and high dietary calcium intakes. , 1980, The Journal of nutrition.

[52]  A. Alfrey,et al.  Renal toxicity of phosphate in rats. , 1980, Kidney international.

[53]  O. Bijvoet,et al.  NOMOGRAM FOR DERIVATION OF RENAL THRESHOLD PHOSPHATE CONCENTRATION , 1975, The Lancet.

[54]  Pochi,et al.  Biochemical Response of Late Rickets and Osteomalacia to a Chupatty-free Diet , 1972, British medical journal.

[55]  R. C. Macridis A review , 1963 .

[56]  E. Mellanby The rickets‐producing and anti‐calcifying action of phytate , 1949, The Journal of physiology.

[57]  E. Mellanby,et al.  Phytic acid and the rickets-producing action of cereals. , 1939, The Biochemical journal.

[58]  M. Razzaque,et al.  Endocrine Regulation of Phosphate Homeostasis , 2018 .

[59]  M. Vervloet,et al.  The role of phosphate in kidney disease , 2017, Nature Reviews Nephrology.

[60]  R. Elashoff,et al.  Early skeletal and biochemical alterations in pediatric chronic kidney disease. , 2012, Clinical journal of the American Society of Nephrology : CJASN.

[61]  H. Jüppner,et al.  Endocrine Regulation of Phosphate Homeostasis , 2009 .

[62]  T. Oh,et al.  Ca(2+)-inositol phosphate chelation mediates the substrate specificity of beta-propeller phytase. , 2006, Biochemistry.

[63]  B. Beck,et al.  Cross-sectional study , 2011 .

[64]  Dr. F. D’Alessandro A Modern Perspective , 2003 .

[65]  T. Oh,et al.  Biochemical properties and substrate specificities of alkaline and histidine acid phytases , 2003, Applied Microbiology and Biotechnology.

[66]  J. March,et al.  Phytate prevents tissue calcifications in female rats , 2000, BioFactors.

[67]  Z. Herman,et al.  Lowering of serum cholesterol and triglycerides and modulation of divalent cations by dietary phytate. , 1990 .

[68]  P. Restani,et al.  Evaluation of the oral toxicity of spinacine hydrochloride in a 13-week study in rats. , 1989, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[69]  D. Fraser,et al.  A new mechanism for induced vitamin D deficiency in calcium deprivation , 1987, Nature.

[70]  D. K. Salunkhe,et al.  Phytates in legumes and cereals. , 1982, Advances in food research.

[71]  J. A. Bey The British Industrial Biological Research Association , 1960, Nature.