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Role of Phosphate in Biomineralization Henry Ford Health System Henry Ford Health System Scholarly Commons Endocrinology Articles Endocrinology and Metabolism 7-25-2020 Role of Phosphate in Biomineralization Sanjay Kumar Bhadada Sudhaker D. Rao Henry Ford Health System, [email protected] Follow this and additional works at: https://scholarlycommons.henryford.com/endocrinology_articles Recommended Citation Bhadada SK, and Rao SD. Role of Phosphate in Biomineralization. Calcif Tissue Int 2020. This Article is brought to you for free and open access by the Endocrinology and Metabolism at Henry Ford Health System Scholarly Commons. It has been accepted for inclusion in Endocrinology Articles by an authorized administrator of Henry Ford Health System Scholarly Commons. Calcifed Tissue International https://doi.org/10.1007/s00223-020-00729-9 REVIEW Role of Phosphate in Biomineralization Sanjay Kumar Bhadada1 · Sudhaker D. Rao2,3 Received: 31 March 2020 / Accepted: 14 July 2020 © Springer Science+Business Media, LLC, part of Springer Nature 2020 Abstract Inorganic phosphate is a vital constituent of cells and cell membranes, body fuids, and hard tissues. It is a major intracel- lular divalent anion, participates in many genetic, energy and intermediary metabolic pathways, and is important for bone health. Although we usually think of phosphate mostly in terms of its level in the serum, it is needed for many biological and structural functions of the body. Availability of adequate calcium and inorganic phosphate in the right proportions at the right place is essential for proper acquisition, biomineralization, and maintenance of mass and strength of the skeleton. The three specialized mineralized tissues, bones, teeth, and ossicles, difer from all other tissues in the human body because of their unique ability to mineralize, and the degree and process of mineralization in these tissues also difer to suit the specifc functions: locomotion, chewing, and hearing, respectively. Biomineralization is a dynamic, complex, and lifelong process by which precipitations of inorganic calcium and inorganic phosphate divalent ions form biological hard tissues. Understanding the biomineralization process is important for the management of diseases caused by both defective and abnormal mineralization. Hypophosphatemia results in mineralization defects and osteomalacia, and hyperphosphatemia is implicated in abnormal excess calcifcation and/or ossifcation, but the exact mechanisms underlying these processes are not fully understood. In this review, we summarize available evidence on the role of phosphate in biomineralization. Other manuscripts in this issue of the journal deal with other relevant aspects of phosphate homeostasis, phosphate signaling and sensing, and disorders resulting from hypo- and hyperphosphatemic states. Keywords Biomineralization · Hypophosphatemia · Hyperphosphatemia · Vascular calcifcation · Soft tissue calcifcation · Calciphylaxis · Enthesopathy · Heterotopic ossifcation Introduction bones and teeth [4], the two hardest tissues in human body. Among the various micronutrients in bone, Ca and Pi are Phosphate (Pi) is a vital constituent of cells and cell mem- the two major components of hydroxyapatite, the crystalline branes as well as of body fuids and tissues, it is a major mineral component of the extracellular organic matrix of intracellular divalent anion, participates in many genetic, bone. Phosphate metabolism, distribution, intracellular sign- energy and intermediary metabolic pathways, and is impor- aling, physiological and pathological perturbations causing tant for bone health [1–3]. Availability of calcium (Ca) and hypo- and hyperphosphatemia, and clinical aspects of phos- inorganic phosphate (Pi) in the right proportions at the right phate excess and depletion are dealt with in other sections place is crucial for proper acquisition, biomineralization of in this issue of the journal. Accordingly, in this section, we collagen fbrils, and maintenance of mass and strength of will focus exclusively on the role of phosphate in biomin- eralization, and more specifcally, in bone and other tissue mineralization. A knowledge and understanding the role of * Sudhaker D. Rao phosphate in biomineralization processes are essential to [email protected] manage patients with disorders of phosphate metabolism 1 Department of Endocrinology, PGIMER, Chandigarh, India and the associated abnormal biomineralization of bone and 2 Division of Endocrinology, Diabetes, and Bone & Mineral other tissues. Disorders, Henry Ford Hospital, New Center One; Suite # 800, Detroit, MI 48202, USA 3 Bone & Mineral Research Laboratory, Henry Ford Hospital, Detroit, MI, USA Vol.:(0123456789)1 3 S. K. Bhadada, S. D. Rao Distribution and Role of Phosphate tissues such as bone, cementum, dentin, and enamel [8, 9]. in the Body Understanding the biomineralization process is important for the management of diseases caused by both defective Although we think of phosphate mostly in terms of its and abnormal mineralization [10–15]. Throughout life level in the serum, which is maintained within a narrow bone and teeth, but not ossicles, are subject to processes range for many biological and structural functions of the of mineralization and demineralization on a constant and body, phosphate is also an integral part of bones, tissues, continual basis required for renovation of these hard tis- cells and cell membranes. In a typical Western diet con- sues [9]. Notwithstanding the signifcant progress made tains 1000–1600 mg of Pi/day, of which 3 mg/kg body- in our understanding of bone biology several questions weight/day enters the extracellular fuid with consequent remain: What are the initial steps in biomineralization? exchange with bone as required [5, 6]. Bone contains about How is the temporal and spatial regulation of matrix 99 and 80% of the total body content of Ca and Pi with a production and biomineralization integrated and accom- mass ratio of 2:2. Both these divalent ions exist in soluble plished? Why does biologic mineralization normally occur and semi-soluble form in body fuids, cells and cell mem- only in certain types of tissues but not in others? Why, branes, and phosphate circulates in the blood in free form, and under what circumstances, does abnormal biominer- bound to protein, and as complex with Ca. A 70 kg individ- alization occur? Is non-skeletal biomineralization such as ual has approximately 500–800 g of total body phosphate, that occurs in muscles, tendons, cartilage, and blood ves- 80% of which is in the form of hydroxyapatite crystal in sels dependent on ambient Pi or due to underlying tissue bone and 20% as intracellular component. Intracellularly, characteristics? Are any other cells involved in biominer- phosphate is present predominantly in the organic form in alization besides the osteogenic cells? Nevertheless, con- nucleic acids and nucleoproteins. In contrast, both organic sidering that mineralized hard tissue formation in vivo is and inorganic forms of phosphate are present in serum, the governed by a combination of cellularly driven processes latter is measured routinely by standard methods in clini- and thermodynamics, biomineralization should be consid- cal laboratories. At physiological pH of 7.40, phosphate ered both biological and chemical in nature [16]. exists as a mixture of ions (orthophosphates): HPO 2− and Phosphate, Ca and type-1 collagen fbrils are the major 4− H2PO in a ratio of 4:1. Normal physiological functions building blocks of bone tissue aided by key enzymes of phosphate are manifold: it is the major source of high [17–20]. In humans, free phosphates also have control over energy phosphate bonds (ATP) required ubiquitously the formation of new mineral by infuencing a wide variety for cellular homeostasis-muscle contraction, electrolyte of cells (chondrocytes, osteoblasts, and osteocytes), signal- transport, etc.; it is an integral part of intracellular mes- ing molecules, and enzymes [16] (see other chapters in this senger system including cyclic adenosine and guanosine issue). Not surprisingly serum phosphate concentrations monophosphates (c-AMP; c-GMP); it is required, for the vary considerably with age, higher in infants and children synthesis phospholipid bilayer of all cell membranes; it is (1.5–2.65 mM) and decline during adulthood (0.8–1.5 mM) involved in the formation of 2,3-diphosphoglycerol that [21]. This is most likely because of higher requirements for regulates oxygen delivery to tissues, and acts as a bufer phosphate needed for bone growth, optimal bone mineraliza- to maintain normal blood pH and plays a signifcant role in tion, and to achieve peak bone mass in infants and growing immune functions and coagulation cascade (also see other children. chapters in this issue). The frst step in biomineralization process, at least in bone, appears to be the nucleation of Ca–Pi crystals within the matrix vesicles (Fig. 1) [4, 22, 23], followed by formation of amorphous Ca–Pi (ACP) phase with gradual transition to The Process of Biomineralization Ca–Pi crystal nucleation resulting in hydroxyapatite crys- tal [4, 24]. The Ca–Pi crystal nucleation takes place within The three most mineralized tissues (bones, teeth, and ossi- the matrix vesicles that bud from the plasma membrane of cles) are specialized organs that difer from all other tis- osteogenic cells [25]. The matrix vesicles are endowed with sues in the human body because of their unique ability to two key enzymes, tissues non-specifc alkaline phosphatase mineralize [7, 8]. Interestingly,
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