Source: OKLAHOMA STATE UNIVERSITY submitted to NRP
MICROARCHITECTURAL, STRUCTURAL, AND CELLULAR ALTERATIONS IN BONE: ROLE OF IRON IN MAINTAINING OPTIMAL BONE HEALTH
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
0219206
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Aug 1, 2009
Project End Date
Sep 30, 2011
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
OKLAHOMA STATE UNIVERSITY
(N/A)
STILLWATER,OK 74078
Performing Department
Human Sciences
Non Technical Summary
Diseases of iron metabolism continue to be a major health concern with iron deficiency remaining the most common single nutrient deficiency in the U.S. Inadequate dietary iron can result in iron deficiency anemia, characterized by impaired oxygen transport, and is associated with lethargy, decreased work capacity, and impaired development of motor and cognitive skills in children. Iron status is also associated with the development of chronic diseases such as cardiovascular disease, diabetes, and osteoporosis. At present little is known as to how iron deficiency during adolescence affects the risk for chronic diseases affecting the cardiovascular, neurological, and musculoskeletal systems later in life. Osteoporosis affects nearly half of all women over the age of 50 resulting in fractures that are both debilitating and costly. Despite the use of effective drug therapies, this disease continues to be a significant public health concern. The most important factor influencing an individual?s predisposition for osteoporosis-related fractures is their peak bone mass, which is generally acquired between the ages of 25 and 35 years. Once peak bone mass is achieved, bone loss is an inevitable part of the aging process. Factors such as nutritional status and physical activity, which are key determinants in the acquisition of bone mass, likely play a critical role in an individual?s lifetime risk for osteoporosis. Studies have demonstrated that iron deficiency worsens calcium deficiency by further decreasing bone mass, strength, and structure in young animals. The mechanism underlying these observations remains unclear but may be related to the essential role of iron as a cofactor for enzymes promoting quality bone formation. Nutrient deficiencies and amenorrhea are common problems in young female athletes and may contribute significantly to stress fractures and future osteoporosis risk. These data from animal and human studies indicate that iron deficiency has a significant impact on bone quality. Since high levels of iron also negatively affect bone health, it indicates how little we know about the role of iron in bone metabolism and supports the need for a more in-depth examination of the role of iron in maintaining optimal bone health. Using an animal model of iron deficiency we will examine how a lack of dietary iron negatively affects bone health by examining structural properties of bone in addition to examining the expression of genes associated with bone metabolism. Using a combination of in vivo and in vitro experiments, we will assess the role of iron in regulating the development of cells required for proper bone metabolism. The results of these studies will further our understanding of the role of iron in the maintenance of skeletal health and will provide information to the scientific community that will enhance our understanding of the long-term implications of iron deficiency. Further, the results may be useful for providing evidence to consumers that anemia has consequences well beyond malaise and decreased work capacity, and may contribute to the development of chronic disease.
Animal Health Component
(N/A)
Research Effort Categories
Basic
(N/A)
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
7023840101050%
7025010101050%
Goals / Objectives
The long-term goal of our laboratory is to advance understanding how iron metabolism is coordinated, and how alterations in iron sensing can lead to the development of disease. This accords with the DASNR high priority Team Initiative Program area in Human Nutrition and Health with a focus on improving nutritional status. Our primary objectives are to determine the extent to which iron status affects skeletal development during a period of rapid growth and to assess the relationship between cellular iron status and the dynamic processes of bone formation and bone resorption at a cellular level. The central hypothesis is that dietary iron deficiency alters bone density and quality by negatively regulating the development of bone forming and resorptive precursor cells (osteoblasts and osteoclasts, respectively) responsible for normal bone development. This hypothesis is based on observations that (1) iron deficiency is associated with decreases in bone quality and strength, and (2) differentiation of osteoblastic and osteoclastic precursors in cell culture is iron-regulated. Our rationale is that determination of the role(s) of iron in modulating bone physiology will provide novel fundamental insight into the understanding of how an inadequate iron status may affect the accumulation of peak bone mass and increase the risk of developing osteoporosis. This research will enable us to refine models of how iron regulates such diverse processes as oxygen transport, energy metabolism, and skeletal development. Furthermore, the results of this project will provide important preliminary data for future extramural grant applications and establish our collaborative efforts through peer-review publication. This proposal builds on previous research and results, allowing to the PI to address objectives at both the whole animal and cellular level, and encompasses two specific aims: (1) To determine the extent to which dietary iron deficiency affects bone mineral density and bone microarchitecture during a period of rapid growth, and (2) To examine the relationship between cellular iron status and the differentiation of osteoblastic and osteoclastic precursors. This research explores the relationship between iron status and maintenance of optimal bone health. Upon completion of this research we will have provided key insights into the mechanisms through which alterations in cellular iron status alter the dynamics of bone formation and resorption. Furthermore, by providing evidence of the expanding roles of iron in maintaining optimal health, we will make significant contributions to defining the extent to which a compromised iron status may have long-term consequences in terms of osteopenia and/or osteoporosis. Advancing current understanding of the iron-dependent physiological response to iron deficiency will significantly inform understanding of mechanisms coordinating whole-body iron metabolism. Given the prevalence of this single nutrient deficiency among young women during a period of key skeletal development, the broader impact of this research includes critical new understanding of iron's role in maintaining optimal health among Oklahoma citizens.
Project Methods
The first aim will allow us to test the hypothesis that dietary iron deficiency during a period of rapid growth negative regulates bone density and microarchitecture. Weanling 22 day old female Sprague-Dawley rats weighing approximately 50 g will be housed at the OSU Laboratory Animal Research Facility. Animals will be provided either a control (C, n = 8; 50 mg Fe/kg diet) or iron-deficient (ID, n = 8; 3-5 mg Fe/kg diet) diet for 28 days. To control for differences in total intake, we will also include a pair-fed group (PF, n = 8) that will receive the control diet at the level of intake as that of the ID group. The degree of anemia will be assessed by measuring hemoglobin concentration and reticulocyte number in heparinized arterial blood. Alterations in bone mineral area, content, and density associated with iron deficiency will be assessed by dual-energy x-ray absorptiometry (DXA) scans. Assessment of trabecular and cortical bone microarchitecture is an important measure for characterizing the effects of iron on bone acquisition during growth. Images of the tibia will be obtained using micro-computed tomography and will provide detailed structural information related to trabecular and cortical bone and will enable us to determine the extent to which iron deficiency alters bone structure. To examine iron-dependent changes in gene expression in bone, we will extract femoral RNA from rats at the completion of the study period. Total RNA will be reverse-transcribed and cDNA used to examine gene expression by high-throughput real-time PCR. Using gene expression as a surrogate marker of cell type, we will assess relative changes in population in response to iron deficiency. We expect to find that iron deficiency alters the populations of both osteoblastic and osteoclastic precursors. These results will aid us in determining how iron affects cell-specific activities and the implications of iron deficiency on bone metabolism. Additionally, we will harvest bone marrow cells from these same animals and purify both osteoblastic and osteoclastic cells that will allow us to more accurately assess changes in gene expression in response to iron deficiency in an individual cell-type to determine how iron may alter osteoblastic or osteoclastic activity. We expect that iron deficient animals will have less bone mineral density when compared to pair-fed controls, indicating specifically that the lack of dietary iron adversely affects overall mineral accretion in rapidly growing animals. We expect that dietary iron deficiency decreases bone quality as measured by changes in trabecular spacing, thickness, number, and volume. These results will demonstrate that even in the presence of adequate calcium, a lack of dietary iron adversely affects not only bone mineral density, but also bone microarchitecture. Lastly, by examining iron-dependent changes in gene expression in the bone, we will be able to narrow our focus to the possible cell types that may be preferentially affected in dietary iron deficiency.

Progress 08/01/09 to 09/30/11

Outputs
OUTPUTS: Over the previous 12 months, the results of an additional study utilizing an animal model of dietary iron deficiency have been collected and are continuing to be analyzed. In this additional study, animals were provided an iron deficient diet for 21 and 35 days after which tissues were collected to examine iron status and the impact of inadequate dietary iron on bone health. Animals were fed diets based on either the AIN-76 or AIN-93 diet mix to assess the extent to which dietary carbohydrate may interact with iron deficiency to increase the risk of bone loss. We have completed analysis of tissues from this most recent study and presented these findings at a poster session at the 2011 American Society for Bone and Mineral Research Annual Meeting in San Diego, CA. Also, a poster detailing the results of the first study was presented at the Oklahoma Dietetic Association annual Spring meeting in 2011. We are currently completing the preparation of a manuscript detailing these results and expect to submit this paper for reviewing. PARTICIPANTS: Dr. Stephen Clarke (PI): Designed, implemented, and directed project; Responsible for the data collection/analysis and preparation of presentation/manuscripts; Mentored undergraduate and graduate students. Krista M. Shawron, MS, RD: Conducted animal experiments; Assisted in data collection/analysis and preparation of presentation/manuscripts; Assisted in the mentoring of undergraduate research scholars. Kristen K. Hester (Graduate Student); Assisted with animal experiments and data collection/analysis. Both the PI and graduate students were afforded the opportunity to gain additional training in advanced methods of analysis of calcified tissue (e.g., bone). TARGET AUDIENCES: The primary audience for the work is the scientific community involved in micronutrient and osteoporosis research. We expect that the findings of this project will provide insight into the role of iron deficiency in increasing fracture risk in affected populations. Provided the increase in osteoporosis and the prevalence of iron deficiency, it is essential that we develop a deeper understanding of the role of micronutrients in promoting optimal skeletal health. Data, results, and conclusions from the project were presented to colleagues and students at the Annual Meeting of the American Society for Bone and Mineral Research. Additionally, the project has allowed undergraduate research scholars to gain experience in conducting science experiments and to attend and interact in weekly laboratory meetings. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
As a result of the experiments that have been conducted, our laboratory has now expanded our understanding of the role of iron in maintaining optimal bone health thereby potentially limiting a risk factor for the development of osteoporosis and other chronic diseases. We are particularly interested in the extent to which an inadequate iron status impairs bone formation in a developing animal and believe that these results may have important implications with respect to periods of rapid bone growth during adolescence. We have shared our finding with the greater scientific community through poster presentations and expect that these results will be submitted for publication in the coming months.

Publications

  • Dietary Iron Deficiency is Associated with Impaired Mineralization and Osteogenic Gene Expression in Weanling Sprague-Dawley Rats. Krista M. Shawron, McKale R. Davis, Elizabeth Rendina, Yan Wang, Edralin A. Lucas, Brenda J. Smith, and Stephen L. Clarke. Department of Nutritional Sciences, Oklahoma State University, Stillwater, OK. Presentation Number SU0399, American Society for Bone and Mineral Research Annuak Meeting, San Diego, CA, September 18, 2011.


Progress 10/01/09 to 09/30/10

Outputs
OUTPUTS: ACTIVITIES: Over the previous 12 months, two individual studies utilizing an animal model of dietary iron deficiency have been conducted. In the first study (November 2009), animals were provided an iron deficient diet for 35 days after which tissues were collected to examine iron status and the impact of inadequate dietary iron on bone health. More recently, we completed a second animal study and are in the process of beginning to analyze tissue samples for this experiment. DISEMMINATION: We have completed analysis of tissues from this first study and presented these findings at a poster session at the 2010 American Society for Bone and Mineral Research Annual Meeting in Toronto, Canada. We anticipate that the preparation and submission of a manuscript within 6 months. PARTICIPANTS: Dr. Stephen Clarke (PI): Designed, implemented, and directed project; Responsible for the data collection/analysis and preparation of presentation/manuscripts; Mentored undergraduate and graduate students. Krista M. Shawron (Graduate Student): Conducted animal experiments; Assisted in data collection/analysis and preparation of presentation/manuscripts; Assisted in the mentoring of undergraduate research scholars. TRAINING OR PROFESSIONAL DEVELOPMENT: The PI and graduate student were afforded the opportunity to gain additional training in advanced methods of analysis of calcified tissue (e.g., bone). TARGET AUDIENCES: The primary audience for the project is the scientific community involved in micronutrient and osteoporosis research. We expect that the findings of this project will provide insight into the role of iron deficiency in increasing fracture risk in affected populations. Provided the increase in osteoporosis and the prevalence of iron deficiency, it is essential that we develop a deeper understanding of the role of micronutrients in promoting optimal skeletal health. EFFORTS: Data, results, and conclusions from the project were presented to colleagues and students at the 2010 Annual Meeting of the American Society for Bone and Mineral Research. Additionally, the project has allowed undergraduate research scholars to gain experience in conducting science experiments and to attend and interact in weekly laboratory meetings. PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
CHANGE IN KNOWLEDGE: As a result of the experiments being conducted, our laboratory has now expanded our understanding of the role of iron in maintaining optimal bone health thereby potentially limiting a risk factor for the development of osteoporosis and other chronic diseases. We have shared our finding with the greater scientific community through a poster presentation and expect that these results will be submitted for publication in the coming months.

Publications

  • Iron Deficiency Negatively Affects Spine Bone Mineral Density and Bone Microarchitecture in Weanling Sprague Dawley Rats. Krista Shawron, McKale Davis, Elizabeth Rendina, Yan Wang, Edralin Lucas, Brenda Smith, and Stephen Clarke, Oklahoma State University, USA, Presentation Number: MO0359. American Society for Bone and Mineral Research 2010 Annual Meeting, Toronto, Canada, October 18, 2010


Progress 10/01/08 to 09/30/09

Outputs
OUTPUTS: This project was new to PI in Aug. 2009 so there is nothing of significance to report this period. PARTICIPANTS: Nothing significant to report during this reporting period. TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
This project was new to PI in Aug. 2009 so there is nothing of significance to report this period.

Publications

  • No publications reported this period